Philippa Kaur

1.Andersson, M. B. Sexual Selection (Princeton University Press, 1994).Book 

Google Scholar 
2.Royle, N. J., Smiseth, P. T. & Kölliker, M. The Evolution of Parental Care (Oxford University Press, 2012).Book 

Google Scholar 
3.Herridge, E. J., Murray, R. L., Gwynne, D. T. & Bussière, L. F. Mating and parental sex roles, diversity in. Encycl. Evol. Biol. 2, 453–458 (2016).Article 

Google Scholar 
4.Kokko, H. & Jennions, M. D. Parental investment, sexual selection and sex ratios. J. Evol. Biol. 21, 919–948 (2008).PubMed 
Article 
PubMed Central 

Google Scholar 
5.Schärer, L., Rowe, L. & Arnqvist, G. Anisogamy, chance and the evolution of sex roles. Trends Ecol. Evol. 27, 260–264 (2012).PubMed 
Article 
PubMed Central 

Google Scholar 
6.Liker, A., Freckleton, R. P. & Székely, T. The evolution of sex roles in birds is related to adult sex ratio. Nat. Commun. 4, 1–6 (2013).Article 
CAS 

Google Scholar 
7.Jennions, M. D. & Fromhage, L. Not all sex ratios are equal: The Fisher condition, parental care and sexual selection. Philos. Trans. R. Soc. B Biol. Sci 372, 20160312 (2017).Article 

Google Scholar 
8.Darwin, C. The Descent Man, and Selection in Relation to Sex. John Murray, vol. ah-king (1871).9.Ah-King, M. & Ahnesjö, I. The ‘sex role’ concept: An overview and evaluation. Evol. Biol. 40, 461–470 (2013).Article 

Google Scholar 
10.Pizzari, T. & Bonduriansky, R. Sexual behaviour: Conflict, cooperation and co-evolution. In Social Behaviour: Genes, Ecology and Evolution (eds Szekely, T. et al.) (Cambridge University Press, 2010).
Google Scholar 
11.Trumbo, S. T. Patterns of parental care in invertebrates. Evol. Parent. Care 12, 62–81 (2012).
Google Scholar 
12.Balshine, S. Patterns of parental care in vertebrates. In The Evolution of Parental Care (eds Royle, N. et al.) 62–81 (Oxford University Press, 2012).Chapter 

Google Scholar 
13.Székely, T., Remeš, V., Freckleton, R. P. & Liker, A. Why care? Inferring the evolution of complex social behaviour. J. Evol. Biol. 26, 1381–1391 (2013).PubMed 
Article 
PubMed Central 

Google Scholar 
14.Bateman, A. J. Intra-sexual selection in Drosophila. Heredity 2, 349–368 (1948).PubMed 
Article 
CAS 
PubMed Central 

Google Scholar 
15.Snyder, B. F. & Gowaty, P. A. A reappraisal of Bateman’s classic study of intrasexual selection. Evolution 61, 2457–2468 (2007).PubMed 
Article 
PubMed Central 

Google Scholar 
16.Gowaty, P. A., Kim, Y.-K. & Anderson, W. W. No evidence of sexual selection in a repetition of Bateman’s classic study of Drosophila melanogaster. Proc. Natl. Acad. Sci. 109, 11740–11745 (2012).PubMed 
PubMed Central 
Article 
ADS 

Google Scholar 
17.Wade, M. J. Don’t Throw Bateman Out with the Bathwater!. Integr. Comp. Biol. 45, 945–951 (2005).PubMed 
Article 
PubMed Central 

Google Scholar 
18.Dewsbury, D. A. The Darwin–Bateman paradigm in historical context. Integr. Comp. Biol. 45, 831–837 (2005).PubMed 
Article 
PubMed Central 

Google Scholar 
19.Parker, G. A. The sexual cascade and the rise of pre-ejaculatory (Darwinian) sexual selection, sex roles, and sexual conflict. Cold Spring Harb. Lab. Press 6, a017509 (2014).Article 

Google Scholar 
20.Jones, A. G., Arguello, J. R. & Arnold, S. J. Validation of Bateman’s principles: A genetic study of sexual selection and mating patterns in the rough-skinned newt. Proc. R. Soc. B Biol. Sci. 269, 2533–2539 (2002).Article 

Google Scholar 
21.Collet, J. M., Dean, R. F., Worley, K., Richardson, D. S. & Pizzari, T. The measure and significance of Bateman’s principles. Proc. R. Soc. B Biol. Sci. 281, 20132973–20132973 (2014).Article 

Google Scholar 
22.Hoquet, T. Bateman (1948): Rise and fall of a paradigm?. Anim. Behav. https://doi.org/10.1016/j.anbehav.2019.12.008 (2019).Article 

Google Scholar 
23.Janicke, T., Häderer, I. K., Lajeunesse, M. J. & Anthes, N. Darwinian sex roles confirmed across the animal kingdom. Sci. Adv. 2, e1500983–e1500983 (2016).PubMed 
PubMed Central 
Article 
ADS 

Google Scholar 
24.Tang-Martinez, Z. & Ryder, B. T. The problem with paradigms: Bateman’s worldview as a case study. Integr. Comp. Biol. 54, 821–830 (2005).Article 

Google Scholar 
25.Levitan, D. Does Bateman’s principle apply to broadcast-spawning organisms ? Egg traits Iifluence in situ fertilization rates among congeneric sea urchins. Evolution 52, 1043–1056 (1998).PubMed 

Google Scholar 
26.Drea, C. M. Bateman revisited: The reproductive tactics of female primates. Integr. Comp. Biol. 45, 915–923 (2005).PubMed 
Article 

Google Scholar 
27.Kokko, H. Should advertising parental care be honest?. Proc. R. Soc. B Biol. Sci. 265, 1871–1878 (1998).Article 

Google Scholar 
28.Remeš, V. & Matysioková, B. More ornamented females produce higher-quality offspring in a socially monogamous bird: An experimental study in the great tit (Parus major). Front. Zool. 10, 1–10 (2013).Article 

Google Scholar 
29.Hanschen, E. R., Herron, M. D., Wiens, J. J., Nozaki, H. & Michod, R. E. Multicellularity drives the evolution of sexual traits. Am. Nat. 192, E93–E105 (2018).PubMed 
PubMed Central 
Article 

Google Scholar 
30.Queller, D. C. Why do females care more than males?. Proc. R. Soc. B Biol. Sci. 264, 1555–1557 (1997).Article 
ADS 

Google Scholar 
31.Alcock, J. Sexual selection and the mating behavior of solitary bees. in (eds. Brockmann, H. J. et al.) vol. 45 1–48 (Academic Press, 2013).32.Bjork, A. & Pitnick, S. Intensity of sexual selection along the anisogamy–isogamy continuum. Nature 441, 742–745 (2006).PubMed 
Article 
ADS 
CAS 
PubMed Central 

Google Scholar 
33.Kodric-Brown, A. & Brown, J. H. Anisogamy, sexual selection, and the evolution and maintenance of sex. Evol. Ecol. 1, 95–105 (1987).Article 

Google Scholar 
34.Schulte-Hostedde, A. I., Millar, J. S. & Gibbs, H. L. Sexual selection and mating patterns in a mammal with female-biased sexual size dimorphism. Behav. Ecol. 15, 351–356 (2004).Article 

Google Scholar 
35.Liker, A., Freckleton, R. P., Remeš, V. & Székely, T. Sex differences in parental care: Gametic investment, sexual selection, and social environment. Evolution 69, 2862–2875 (2015).PubMed 
Article 
PubMed Central 

Google Scholar 
36.Bjork, A. & Pitnick, S. Intensity of sexual selection along the anisogamy-isogamy continuum. Nature 441, 742–745 (2006).PubMed 
Article 
ADS 
CAS 
PubMed Central 

Google Scholar 
37.Thomas, G. H. & Székely, T. Evolutionary pathways in shorebird breeding systems: Sexual conflict, parental care, and chick development. Evolution 59, 2222 (2006).Article 

Google Scholar 
38.Gonzalez-Voyer, A., Fitzpatrick, J. L. & Kolm, N. Sexual selection determines parental care patterns in cichlid fishes. Evolution 62, 2015–2026 (2008).PubMed 
Article 
PubMed Central 

Google Scholar 
39.Garamszegi, L. Z. & Møller, A. P. Untested assumptions about within-species sample size and missing data in interspecific studies. Behav. Ecol. Sociobiol. 66, 1363–1373 (2012).Article 

Google Scholar 
40.Nakagawa, S. & Freckleton, R. P. Model averaging, missing data and multiple imputation: A case study for behavioural ecology. Behav. Ecol. Sociobiol. 65, 103–116 (2011).Article 

Google Scholar 
41.Nakagawa, S. & Freckleton, R. P. Missing inaction: The dangers of ignoring missing data. Trends Ecol. Evol. 23, 592–596 (2008).PubMed 
Article 
PubMed Central 

Google Scholar 
42.Wiens, J. J. & Morrill, M. C. Missing data in phylogenetic analysis: Reconciling results from simulations and empirical data. Syst. Biol. 60, 719–731 (2011).PubMed 
Article 
PubMed Central 

Google Scholar 
43.Apakupakul, K. & Rubenstein, D. R. Bateman’s principle is reversed in a cooperatively breeding bird. Biol. Lett. 11, 20150034 (2015).PubMed 
PubMed Central 
Article 

Google Scholar 
44.Nakagawa, S. et al. Meta-analysis of variation: Ecological and evolutionary applications and beyond. Methods Ecol. Evol. 6, 143–152 (2015).Article 

Google Scholar 
45.Lajeunesse, M. Recovering missing data or partial data from studies: A survey of conversions and imputation for meta-analysis. Handb. Meta-Anal. Ecol. Evol. 195–206 (2013).46.Smith, R. J. Statistics of sexual size dimorphism. J. Hum. Evol. 36, 423–458 (1999).PubMed 
Article 
CAS 
PubMed Central 

Google Scholar 
47.Dunn, P. O., Whittingham, L. A. & Pitcher, T. E. Mating systems, sperm competition, and the evolution of sexual dimorphism in birds. Evolution 55, 161–175 (2001).PubMed 
Article 
CAS 
PubMed Central 

Google Scholar 
48.Pérez-Barbería, F. J., Gordon, I. J. & Pagel, M. The origins of sexual dimorphism in body size in ungulates. Evolution 56, 1276–1285 (2002).PubMed 
Article 
PubMed Central 

Google Scholar 
49.Weckerly, F. W. Sexual-size dimorphism: Influence of mass and mating systems in the most dimorphic mammals. J. Mammal. 79, 33–52 (1998).Article 

Google Scholar 
50.Székely, T., Reynolds, J. D. & Figuerola, J. Sexual size dimorphism in shorebirds, gulls, and alcids: The influence of sexual and natural selection. Evolution 54, 1404–1413 (2000).PubMed 
Article 
PubMed Central 

Google Scholar 
51.Fairbairn, D. J., Blanckenhorn, W. U. & Székely, T. Sex, Size and Gender Roles: Evolutionary Studies of Sexual Size Dimorphism (Oxford University Press, 2007).Book 

Google Scholar 
52.Janicke, T. & Fromonteil, S. Sexual Selection and Sexual Size Dimorphism in Animals. (2021) https://doi.org/10.1101/2021.05.10.443408.53.De Lisle, S. P. Understanding the evolution of ecological sex differences: Integrating character displacement and the Darwin–Bateman paradigm. Evol. Lett. 3, 434–447 (2019).Article 

Google Scholar 
54.Harvey, P. H. & Clutton-Brock, T. H. Life history variation in primates. Evolution 39, 559–581 (1985).PubMed 
Article 
PubMed Central 

Google Scholar 
55.Hedges, S. B., Dudley, J. & Kumar, S. TimeTree: A public knowledge-base of divergence times among organisms. Bioinformatics 22, 2971–2972 (2006).PubMed 
Article 
CAS 
PubMed Central 

Google Scholar 
56.Martins, E. P. & Hansen, T. F. Phylogenies and the comparative method: A general approach to incorporating phylogenetic information into the analysis of interspecific data. Am. Nat. 149, 646–667 (1997).Article 

Google Scholar 
57.Pagel, M. Inferring evolutionary processes from molecular phylogenies. Zool. Scr. 98, 313–333 (1997).
Google Scholar 
58.Freckleton, R. P., Harvey, P. H. & Pagel, M. Phylogenetic analysis and comparative data: A test and review of evidence. Am. Nat. 160, 712–726 (2002).PubMed 
Article 
CAS 
PubMed Central 

Google Scholar 
59.Cooper, N., Thomas, G. H., Venditti, C., Meade, A. & Freckleton, R. P. A cautionary note on the use of Ornstein Uhlenbeck models in macroevolutionary studies. Biol. J. Linn. Soc. 118, 64–77 (2016).Article 

Google Scholar 
60.Orme, D. The caper package: Comparative analysis of phylogenetics and evolution in R. R Package Version 05(2), 1–36 (2013).
Google Scholar 
61.Penone, C. et al. Imputation of missing data in life-history trait datasets: Which approach performs the best?. Methods Ecol. Evol. 5, 1–10 (2014).Article 

Google Scholar 
62.Goolsby, E. W., Bruggeman, J. & Ané, C. Rphylopars: Fast multivariate phylogenetic comparative methods for missing data and within-species variation. Methods Ecol. Evol. 8, 22–27 (2017).Article 

Google Scholar 
63.Goolsby, A. E. W., Bruggeman, J., Ane, C. & Goolsby, M. E. W. Package ‘ Rphylopars ’. (2016).64.Parker, G. A. Sexual selection and sexual conflict. In Sexual Selection and Reproductive Competition in Insects (eds Blum, M. S. & Blum, N. A.) (Academic Press, 1979).
Google Scholar 
65.Trivers, R. L. Social Evolution (Benjamin-Cummings Pub Co, 1985).
Google Scholar 
66.AlRashidi, M., Kosztolányi, A., Shobrak, M., Küpper, C. & Székely, T. Parental cooperation in an extreme hot environment: Natural behaviour and experimental evidence. Anim. Behav. 82, 235–243 (2011).Article 

Google Scholar 
67.Gwynne, D. T. & Simmons, L. W. Experimental reversal of courtship roles in an insect. Nature 346, 172–174 (1990).Article 
ADS 

Google Scholar 
68.Bonnet, X. et al. Sexual dimorphism in steppe tortoises (Testudo horsfieldii): Influence of the environment and sexual selection on body shape and mobility. Biol. J. Linn. Soc. 72, 357–372 (2001).Article 

Google Scholar 
69.Griskevicius, V. et al. The financial consequences of too many men: Sex ratio effects on saving, borrowing, and spending. J. Pers. Soc. Psychol. 102, 69–80 (2012).PubMed 
Article 
PubMed Central 

Google Scholar 
70.Jirotkul, M. Operational sex ratio influences female preference and male-male competition in guppies. Anim. Behav. 58, 287–294 (1999).PubMed 
Article 
CAS 
PubMed Central 

Google Scholar 
71.Liker, A., Freckleton, R. P. & Székely, T. Divorce and infidelity are associated with skewed adult sex ratios in birds. Curr. Biol. 24, 880–884 (2014).PubMed 
Article 
CAS 
PubMed Central 

Google Scholar 
72.Schacht, R., Kramer, K. L., Székely, T. & Kappeler, P. M. Adult sex ratios and reproductive strategies: A critical re-examination of sex differences in human and animal societies. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 372, 20160309 (2017).PubMed 
PubMed Central 
Article 

Google Scholar 
73.Székely, Á. & Székely, T. Human behaviour: Sex ratio and the city. Curr. Biol. 22, 684–685 (2012).Article 
CAS 

Google Scholar 
74.Székely, T., Liker, A., Freckleton, R. P., Fichtel, C. & Kappeler, P. M. Sex-biased survival predicts adult sex ratio variation in wild birds. Proc. R. Soc. B Biol. Sci. 281, 20140342–20140342 (2014).Article 

Google Scholar 
75.Grant, P. R. & Grant, B. R. Adult sex ratio influences mate choice in Darwin’s finches. Proc. Natl. Acad. Sci. U. S. A. 116, 12373–12382 (2019).PubMed 
PubMed Central 
Article 
CAS 

Google Scholar 
76.Procter, D. S., Moore, A. J. & Miller, C. W. The form of sexual selection arising from male-male competition depends on the presence of females in the social environment. J. Evol. Biol. 25, 803–812 (2012).PubMed 
Article 
CAS 
PubMed Central 

Google Scholar 
77.Janicke, T. & Morrow, E. H. Operational sex ratio predicts the opportunity and direction of sexual selection across animals. Ecol. Lett. https://doi.org/10.1111/ele.12907 (2018).Article 
PubMed 
PubMed Central 

Google Scholar 
78.Wolf, K. N. et al. Age-dependent changes in sperm production, semen quality, and testicular volume in the black-footed ferret (Mustela nigripes). Biol. Reprod. 63, 179–187 (2000).PubMed 
Article 
CAS 
PubMed Central 

Google Scholar 
79.Gasparini, C., Marino, I. A. M., Boschetto, C. & Pilastro, A. Effect of male age on sperm traits and sperm competition success in the guppy (Poecilia reticulata). J. Evol. Biol. 23, 124–135 (2009).PubMed 
Article 
PubMed Central 

Google Scholar 
80.Chargé, R., Jalme, M. S., Lacroix, F., Cadet, A. & Sorci, G. Male health status, signalled by courtship display, reveals ejaculate quality and hatching success in a lekking species. J. Anim. Ecol. 79, 843–850 (2010).PubMed 
PubMed Central 

Google Scholar 
81.Ramirez, M. E. V., Le Pennec, M., Dorange, G., Devauchelle, N. & Nonnotte, G. Assessment of female gamete quality in the pacific oyster crassostrea gigas. Invertebr. Reprod. Dev. 36, 73–78 (1999).Article 

Google Scholar 
82.Berger, T. & Horner, C. M. In vivo exposure of female rats to toxicants may affect oocyte quality. Reprod. Toxicol. 17, 273–281 (2003).PubMed 
Article 
CAS 
PubMed Central 

Google Scholar 
83.Dufour, J. J., Fahmy, M. H. & Minvielle, F. Seasonal changes in breeding activity, testicular size, testosterone concentration and seminal characteristics in rams with long or short breeding season. J. Anim. Sci. 58, 416–422 (1984).PubMed 
Article 
CAS 
PubMed Central 

Google Scholar 
84.Gorman, M. R. & Zucker, I. Seasonal adaptations of siberian hamsters: II: Pattern of change in day length controls annual testicular and body weight rhythms. Biol. Reprod. 53, 116–125 (1995).PubMed 
Article 
CAS 
PubMed Central 

Google Scholar 
85.Parker, G. A. & Begon, M. Optimal egg size and clutch size: Effects of environment and maternal Phenotype. Am. Nat. 128, 573–592 (1986).Article 

Google Scholar 
86.Boyce, M. S. & Perrins, C. M. Optimizing great tit clutch size in a fluctuating environment. Ecology 68, 142–153 (1987).Article 

Google Scholar 
87.Tallamy, D. W. Sexual selection and the evolution of exclusive paternal care in arthropods. Anim. Behav. 60, 559–567 (2000).PubMed 
Article 
CAS 
PubMed Central 

Google Scholar 
88.Olson, V. A., Webb, T. J., Freckleton, R. P. & Székely, T. Are parental care trade-offs in shorebirds driven by parental investment or sexual selection?. J. Evol. Biol. 22, 672–682 (2009).PubMed 
Article 
CAS 
PubMed Central 

Google Scholar 
89.Reynolds, J. D. & Székely, T. The evolution of parental care in shorebirds: Life histories, ecology, and sexual selection. Behav. Ecol. 8, 126–134 (1995).Article 

Google Scholar 
90.Balshine-Earn, S. & Earn, D. J. D. On the evolutionary pathway of parental care in mouth-brooding cichlid fish. Proc. R. Soc. B Biol. Sci. 265, 2217–2222 (1998).Article 

Google Scholar 
91.Ah-King, M., Kvarnemo, C. & Tullberg, B. S. The influence of territoriality and mating system on the evolution of male care: A phylogenetic study on fish. J. Evol. Biol. 18, 371–382 (2005).PubMed 
Article 
CAS 

Google Scholar 
92.Székely, T., Webb, J. N. & Cutchill, I. C. Mating patterns, sexual selection and parental care: An integrative approach. Vertebrate Mat. Syst. https://doi.org/10.1142/9789812793584_0008 (2000).Article 

Google Scholar 
93.Trivers, R. L. Parental investment and sexual selection. (1972).94.Keenleyside, M. H. A. Mate desertion in relation to adult sex ratio in the biparental cichlid fish Herotilapia multispinosa. Anim. Behav. 31, 683–688 (1983).Article 

Google Scholar 
95.Alonzo, S. H. Social and coevolutionary feedbacks between mating and parental investment. Trends Ecol. Evol. 25, 99–108 (2010).PubMed 
Article 

Google Scholar 
96.Houston, A. I., Székely, T. & McNamara, J. M. Conflict between parents over care. Trends Ecol. Evol. 20, 33–38 (2005).PubMed 
Article 

Google Scholar 
97.Clutton-Brock, T. H. The Evolution of Parental Care (Princeton University Press, 1991).Book 

Google Scholar 
98.Liker, A. & Szekely, T. Mortality costs of sexual selection and parental care in natural populations of birds. Evolution 59, 890–897 (2005).PubMed 
Article 

Google Scholar 
99.Emlen, S. T. Lek organization and mating strategies in the bullfrog. Behav. Ecol. Sociobiol. 1, 283–313 (1976).Article 

Google Scholar 
100.Weir, L. K., Grant, J. W. A. & Hutchings, J. A. The influence of operational sex ratio on the intensity of competition for mates. Am. Nat. 177, 167–176 (2011).PubMed 
Article 
PubMed Central 

Google Scholar 
101.Orians, G. H. On the evolution of mating systems in birds and mammals. Am. Nat. 103, 589–603 (1969).Article 

Google Scholar 
102.Carmona-Isunza, M. C. et al. Adult sex ratio and operational sex ratio exhibit different temporal dynamics in the wild. Behav. Ecol. 28, 523–532 (2017).
Google Scholar 
103.Wikelski, M., Trillmich, F. & Jun, N. Body size and sexual size dimorphism in marine iguanas fluctuate as a result of opposing natural and sexual selection: An island comparison. Evolution 51, 922–936 (1997).PubMed 
Article 
PubMed Central 

Google Scholar 
104.Székely, T., Freckleton, R. P. & Reynolds, J. D. Sexual selection explains Rensch’s rule of size dimorphism in shorebirds. Proc. Natl. Acad. Sci. 101, 12224–12227 (2004).PubMed 
PubMed Central 
Article 
ADS 

Google Scholar 
105.Kelly, C. D., Bussière, L. F. & Gwynne, D. T. Sexual selection for male mobility in a giant insect with female-biased size dimorphism. Am. Nat. 172, 417–423 (2008).PubMed 
Article 
PubMed Central 

Google Scholar 
106.Kotiaho, J., Alatalo, R. V., Mappes, J. & Parri, S. Sexual selection in a wolf spider: Male drumming activity, body size, and viability. Evolution 50, 1977 (1996).PubMed 
Article 
PubMed Central 

Google Scholar 
107.Cooke, R. S. C., Eigenbrod, F. & Bates, A. E. Projected losses of global mammal and bird ecological strategies. Nat. Commun. 10, 1–8 (2019).Article 
CAS 

Google Scholar 
108.Cooke, R. S. C., Bates, A. E. & Eigenbrod, F. Global trade-offs of functional redundancy and functional dispersion for birds and mammals. Glob. Ecol. Biogeogr. 28, 484–495 (2019).Article 

Google Scholar 
109.Bakewell, A. T., Davis, K. E., Freckleton, R. P., Isaac, N. J. B. & Mayhew, P. J. Comparing life histories across taxonomic groups in multiple dimensions: How mammal-like are insects?. Am. Nat. 195, 70–81 (2020).PubMed 
Article 
PubMed Central 

Google Scholar 
110.del Villalobos-Segura, M. C., García-Prieto, L. & Rico-Chávez, O. Effects of latitude, host body size, and host trophic guild on patterns of diversity of helminths associated with humans, wild and domestic mammals of Mexico. Int. J. Parasitol. Parasites Wildl. 13, 221–230 (2020).PubMed 
PubMed Central 
Article 

Google Scholar 
111.Pandit, P. S. et al. Predicting wildlife reservoirs and global vulnerability to zoonotic Flaviviruses. Nat. Commun. 9, 1–10 (2018).Article 
CAS 

Google Scholar 
112.Rapacciuolo, G. et al. Species diversity as a surrogate for conservation of phylogenetic and functional diversity in terrestrial vertebrates across the Americas. Nat. Ecol. Evol. 3, 53–61 (2019).Article 

Google Scholar 
113.Capdevila, P. et al. Longevity, body dimension and reproductive mode drive differences in aquatic versus terrestrial life-history strategies. Funct. Ecol. 34, 1613–1625 (2020).Article 

Google Scholar 
114.Ellington, E. H. et al. Using multiple imputation to estimate missing data in meta-regression. Methods Ecol. Evol. 6, 153–163 (2015).Article 

Google Scholar 
115.Pollock, L. J. et al. Protecting biodiversity (in all its complexity): New models and methods. Trends Ecol. Evol. 35, 1119–1128 (2020).PubMed 
Article 
PubMed Central 

Google Scholar 
116.Johnson, T. F., Isaac, N. J. B., Paviolo, A. & González-Suárez, M. Handling missing values in trait data. Glob. Ecol. Biogeogr. 30, 51–62 (2021).Article 

Google Scholar 
117.Onkelinx, T., Devos, K. & Quataert, P. Working with population totals in the presence of missing data comparing imputation methods in terms of bias and precision. J. Ornithol. 158, 603–615 (2017).Article 

Google Scholar  More

1.Pond C. Storage. In: Townsend C, Calow P, editors. Physiological ecology. Oxford: Blackwell Scientific; 1981. p. 190–219.2.Chapin FS, Schulze E, Mooney HA. The ecology and economics of storage in plants. Annu Rev Ecol Syst. 1990;21:423–47.Article 

Google Scholar 
3.Moradali MF, Rehm BHA. Bacterial biopolymers: from pathogenesis to advanced materials. Nat Rev Microbiol. 2020;18:195–210.CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
4.Varpe Ø. Life history adaptations to seasonality. Integr Comp Biol. 2017;57:943–60.PubMed 
Article 
PubMed Central 

Google Scholar 
5.Paul EA. Soil microbiology, ecology and biochemistry. 4th ed. Waltham, MA: Academic Press; 2015.6.Becker KW, Collins JR, Durham BP, Groussman RD, White AE, Fredricks HF, et al. Daily changes in phytoplankton lipidomes reveal mechanisms of energy storage in the open ocean. Nat Commun. 2018;9:1–9.Article 
CAS 

Google Scholar 
7.Rothermich MM, Guerrero R, Lenz RW, Goodwin S. Characterization, seasonal occurrence, and diel fluctuation of poly(hydroxyalkanoate) in photosynthetic microbial mats. Appl Environ Microbiol. 2000;66:13.Article 

Google Scholar 
8.Borzi A. Le comunicazioni intracellulari delle Nostochinee. Malpighia. 1887;1:28–74.
Google Scholar 
9.Sherman LA, Meunier P, Colón-López MS. Diurnal rhythms in metabolism: a day in the life of a unicellular, diazotrophic cyanobacterium. Photosynth Res. 1998;58:25–42.CAS 
Article 

Google Scholar 
10.Stuart RK, Mayali X, Boaro AA, Zemla A, Everroad RC, Nilson D, et al. Light regimes shape utilization of extracellular organic C and N in a cyanobacterial biofilm. mBio. 2016;7:e00650–16.CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
11.Allen MM. Cyanobacterial cell inclusions. Annu Rev Microbiol. 1984;38:1–25.CAS 
PubMed 
Article 

Google Scholar 
12.Sanz-Luque E, Bhaya D, Grossman AR. Polyphosphate: a multifunctional metabolite in cyanobacteria and algae. Front Plant Sci. 2020;11:938.PubMed 
PubMed Central 
Article 

Google Scholar 
13.Martin P, Lauro FM, Sarkar A, Goodkin N, Prakash S, Vinayachandran PN. Particulate polyphosphate and alkaline phosphatase activity across a latitudinal transect in the tropical Indian Ocean: polyphosphate in the tropical Indian Ocean. Limnol Oceanogr. 2018;63:1395–406.CAS 
Article 

Google Scholar 
14.Diaz J, Ingall E, Benitez-Nelson C, Paterson D, de Jonge MD, McNulty I, et al. Marine polyphosphate: a key player in geologic phosphorus sequestration. Science. 2008;320:652–5.CAS 
PubMed 
Article 

Google Scholar 
15.Godwin CM, Cotner JB. Aquatic heterotrophic bacteria have highly flexible phosphorus content and biomass stoichiometry. ISME J. 2015;9:2324–7.CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
16.Oehmen A, Lemos P, Carvalho G, Yuan Z, Keller J, Blackall L, et al. Advances in enhanced biological phosphorus removal: From micro to macro scale. Water Res. 2007;41:2271–300.CAS 
PubMed 
Article 

Google Scholar 
17.Dorofeev AG, Nikolaev YuA, Mardanov AV, Pimenov NV. Role of phosphate-accumulating bacteria in biological phosphorus removal from wastewater. Appl Biochem Microbiol. 2020;56:1–14.CAS 
Article 

Google Scholar 
18.Carrondo MA. Ferritins, iron uptake and storage from the bacterioferritin viewpoint. EMBO J. 2003;22:1959–68.CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
19.Canessa P, Larrondo LF. Environmental responses and the control of iron homeostasis in fungal systems. Appl Microbiol Biotechnol. 2013;97:939–55.CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
20.Harrison PM, Arosio P. The ferritins: molecular properties, iron storage function and cellular regulation. Biochim Biophys Acta. 1996;1275:161–203.PubMed 
Article 
PubMed Central 

Google Scholar 
21.Docampo R, Moreno SNJ. Acidocalcisomes. Cell Calcium. 2011;50:113–9.CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
22.Tsednee M, Castruita M, Salomé PA, Sharma A, Lewis BE, Schmollinger SR, et al. Manganese co-localizes with calcium and phosphorus in Chlamydomonas acidocalcisomes and is mobilized in manganese-deficient conditions. J Biol Chem. 2019;294:17626–41.CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
23.Mojzeš P, Gao L, Ismagulova T, Pilátová J, Moudříková Š, Gorelova O, et al. Guanine, a high-capacity and rapid-turnover nitrogen reserve in microalgal cells. Proc Natl Acad Sci USA. 2020;117:32722–30.24.Turner BL. Inositol phosphates in soil: Amounts, forms and significance of the phosphorylated inositol stereoisomers. In: Turner BL, Richardson AE, Mullaney EJ, editors. Inositol phosphates: linking agriculture and the environment. 2007. Wallingford: CABI; 2007. p. 186–206.25.Flemming H-C, Wingender J. The biofilm matrix. Nat Rev Microbiol. 2010;8:623–33.CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
26.Otero A, Vincenzini M. Nostoc (Cyanophyceae) goes nude: Extracellular polysaccharides serve as a sink for reducing power under unbalanced C/N metabolism. J Phycol. 2004;40:74–81.CAS 
Article 

Google Scholar 
27.Wang J, Yu H-Q. Biosynthesis of polyhydroxybutyrate (PHB) and extracellular polymeric substances (EPS) by Ralstonia eutropha ATCC 17699 in batch cultures. Appl Microbiol Biotechnol. 2007;75:871–8.CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
28.Brangarí AC, Fernàndez-Garcia D, Sanchez-Vila X, Manzoni S. Ecological and soil hydraulic implications of microbial responses to stress—a modeling analysis. Adv Water Resour. 2018;116:178–94.Article 

Google Scholar 
29.Pal S, Manna A, Paul AK. Production of poly(β-hydroxybutyric acid) and exopolysaccharide by Azotobacter beijerinckii WDN-01. World J Microbiol Biotechnol. 1999;15:11–6.Article 

Google Scholar 
30.Kuzyakov Y, Blagodatskaya E. Microbial hotspots and hot moments in soil: Concept & review. Soil Biol Biochem. 2015;83:184–99.CAS 
Article 

Google Scholar 
31.Hauschild P, Röttig A, Madkour MH, Al-Ansari AM, Almakishah NH, Steinbüchel A. Lipid accumulation in prokaryotic microorganisms from arid habitats. Appl Microbiol Biotechnol. 2017;101:2203–16.CAS 
PubMed 
Article 

Google Scholar 
32.Wang JG, Bakken LR. Screening of soil bacteria for poly-β-hydroxybutyric acid production and its role in the survival of starvation. Micro Ecol. 1998;35:94–101.CAS 
Article 

Google Scholar 
33.Hanzlíková A, Jandera A, Kunc F. Poly-3-hydroxybutyrate production and changes of bacterial community in the soil. Folia Microbiologica. 1985;30:58–64.Article 

Google Scholar 
34.Iwahara S, Miki S. Production of α-α-trehalose by a bacterium isolated from soil. Agric Biol Chem. 1988;52:867–8.CAS 

Google Scholar 
35.Treseder KK, Lennon JT. Fungal traits that drive ecosystem dynamics on land. Microbiol Mol Biol Rev. 2015;79:243–62.CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
36.López MF, Männer P, Willmann A, Hampp R, Nehls U. Increased trehalose biosynthesis in Hartig net hyphae of ectomycorrhizas. N Phytol. 2007;174:389–98.Article 
CAS 

Google Scholar 
37.Bünemann EK, Smernik RJ, Doolette AL, Marschner P, Stonor R, Wakelin SA, et al. Forms of phosphorus in bacteria and fungi isolated from two Australian soils. Soil Biol Biochem. 2008;40:1908–15.Article 
CAS 

Google Scholar 
38.Genet P, Prevost A, Pargney JC. Seasonal variations of symbiotic ultrastructure and relationships of two natural ectomycorrhizae of beech (Fagus sylvatica/Lactarius blennius var. viridis and Fagus sylvatica/Lactarius subdulcis). Trees. 2000;14:465–74.Article 

Google Scholar 
39.Frey B, Brunner I, Walther P, Scheidegger C, Zierold K. Element localization in ultrathin cryosections of high-pressure frozen ectomycorrhizal spruce roots. Plant Cell Environ. 1997;20:929–37.CAS 
Article 

Google Scholar 
40.Hanzlíkova A, Jandera A, Kunc F. Formation of poly-3-hydroxybutyrate by a soil microbial community during batch and heterocontinuous cultivation. Folia Microbiol. 1984;29:233–41.Article 

Google Scholar 
41.Mason-Jones K, Banfield CC, Dippold MA. Compound‐specific 13C stable isotope probing confirms synthesis of polyhydroxybutyrate by soil bacteria. Rapid Commun Mass Spectrom. 2019;33:795–802.CAS 
PubMed 
Article 

Google Scholar 
42.Hedlund K. Soil microbial community structure in relation to vegetation management on former agricultural land. Soil Biol Biochem. 2002;34:1299–307.CAS 
Article 

Google Scholar 
43.White PM, Potter TL, Strickland TC. Pressurized liquid extraction of soil microbial phospholipid and neutral lipid fatty acids. J Agric Food Chem. 2009;57:7171–7.CAS 
PubMed 
Article 

Google Scholar 
44.Xu X, Thornton PE, Post WM. A global analysis of soil microbial biomass carbon, nitrogen and phosphorus in terrestrial ecosystems: Global soil microbial biomass C, N and P. Glob Ecol Biogeogr. 2013;22:737–49.Article 

Google Scholar 
45.Bååth E. The use of neutral lipid fatty acids to indicate the physiological conditions of soil fungi. Micro Ecol. 2003;45:373–83.Article 
CAS 

Google Scholar 
46.Soliman AH, Radwan SS. Degradation of sterols, triacylglycerol, and phospholipids by soil microorganisms. Zbl Bakt II Abt. 1981;136:420–6.CAS 

Google Scholar 
47.Diakhaté S, Gueye M, Chevallier T, Diallo NH, Assigbetse K, Abadie J, et al. Soil microbial functional capacity and diversity in a millet-shrub intercropping system of semi-arid Senegal. J Arid Environ. 2016;129:71–9.Article 

Google Scholar 
48.Bölscher T, Wadsö L, Börjesson G, Herrmann AM. Differences in substrate use efficiency: impacts of microbial community composition, land use management, and substrate complexity. Biol Fertil Soils. 2016;52:547–59.Article 
CAS 

Google Scholar 
49.Mason-Jones K, Schmücker N, Kuzyakov Y. Contrasting effects of organic and mineral nitrogen challenge the N-Mining Hypothesis for soil organic matter priming. Soil Biol Biochem. 2018;124:38–46.CAS 
Article 

Google Scholar 
50.Muhammadi S, Afzal M, Hameed S. Bacterial polyhydroxyalkanoates-eco-friendly next generation plastic: Production, biocompatibility, biodegradation, physical properties and applications. Green Chem Lett Rev. 2015;8:56–77.Article 
CAS 

Google Scholar 
51.Jose NA, Lau R, Swenson TL, Klitgord N, Garcia-Pichel F, Bowen BP, et al. Flux balance modeling to predict bacterial survival during pulsed-activity events. Biogeosciences. 2018;15:2219–29.CAS 
Article 

Google Scholar 
52.Medeiros PM, Fernandes MF, Dick RP, Simoneit BRT. Seasonal variations in sugar contents and microbial community in a ryegrass soil. Chemosphere. 2006;65:832–9.CAS 
PubMed 
Article 

Google Scholar 
53.Žifčáková L, Větrovský T, Lombard V, Henrissat B, Howe A, Baldrian P. Feed in summer, rest in winter: microbial carbon utilization in forest topsoil. Microbiome 2017;5:1–12.Article 

Google Scholar 
54.Ratcliff WC, Denison RF. Individual-level bet hedging in the bacterium Sinorhizobium meliloti. Curr Biol. 2010;20:1740–4.CAS 
PubMed 
Article 

Google Scholar 
55.Schoch CL, Ciufo S, Domrachev M, Hotton CL, Kannan S, Khovanskaya R, et al. NCBI Taxonomy: a comprehensive update on curation, resources and tools. Database. 2020;2020:baaa062.CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
56.Choi J, Kim S-H. A genome tree of life for the fungi kingdom. Proc Natl Acad Sci USA. 2017;114:9391–6.CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
57.Jun S-R, Sims GE, Wu GA, Kim S-H. Whole-proteome phylogeny of prokaryotes by feature frequency profiles: An alignment-free method with optimal feature resolution. Proc Natl Acad Sci USA. 2010;107:133–8.CAS 
PubMed 
Article 

Google Scholar 
58.Elbahloul Y, Krehenbrink M, Reichelt R, Steinbuchel A. Physiological conditions conducive to high cyanophycin content in biomass of Acinetobacter calcoaceticus strain ADP1. Appl Environ Microbiol. 2005;71:858–66.CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
59.Lillie SH, Pringle JR. Reserve carbohydrate metabolism in Saccharomyces cerevisiae: responses to nutrient limitation. J Bacteriol. 1980;143:1384–94.CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
60.Hall KD, Guo J. Obesity energetics: Body weight regulation and the effects of diet composition. Gastroenterology. 2017;152:1718–27.e3.PubMed 
Article 

Google Scholar 
61.Sala A, Woodruff DR, Meinzer FC. Carbon dynamics in trees: feast or famine? Tree Physiol. 2012;32:764–75.CAS 
PubMed 
Article 

Google Scholar 
62.Varpe Ø, Ejsmond MJ. Trade-offs between storage and survival affect diapause timing in capital breeders. Evol Ecol. 2018;32:623–41.Article 

Google Scholar 
63.Heilmeier H, Freund M, Steinlein T, Schulze E-D, Monson RK. The influence of nitrogen availability on carbon and nitrogen storage in the biennial Cirsium vulgare (Savi) Ten. I. Storage capacity in relation to resource acquisition, allocation and recycling. Plant Cell Environ. 1994;17:1125–31.CAS 
Article 

Google Scholar 
64.Pond CM. Ecology of storage. In: Levin SA, editor. Encyclopedia of biodiversity, 2nd ed. Amsterdam: Academic Press; 2013. p. 23–38.65.McCue MD. Starvation physiology: reviewing the different strategies animals use to survive a common challenge. Comp Biochem Physiol A Mol Integr Physiol. 2010;156:1–18.PubMed 
Article 
CAS 
PubMed Central 

Google Scholar 
66.Donald J, Pannabecker TL. Osmoregulation in desert-adapted mammals. In: Hyndman KA, Pannabecker TL, editors. Sodium and water homeostasis. New York: Springer New York; 2015. p. 191–211.67.Röttig A, Hauschild P, Madkour MH, Al-Ansari AM, Almakishah NH, Steinbüchel A. Analysis and optimization of triacylglycerol synthesis in novel oleaginous Rhodococcus and Streptomyces strains isolated from desert soil. J Biotechnol. 2016;225:48–56.PubMed 
Article 
CAS 

Google Scholar 
68.Bailey AP, Koster G, Guillermier C, Hirst EMA, MacRae JI, Lechene CP, et al. Antioxidant role for lipid droplets in a stem cell niche of Drosophila. Cell. 2015;163:340–53.CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
69.Jenni-Eiermann S, Jenni L. Fasting in birds: general patterns and the special case of endurance flight. In: McCue MD, editor. Comparative physiology of fasting, starvation, and food limitation. 2012. Berlin: Springer; 2012. p. 171–92.70.Fischer B, Dieckmann U, Taborsky B. When to store energy in a stochastic environment. Evolution. 2011;65:1221–32.PubMed 
Article 
PubMed Central 

Google Scholar 
71.Bonnet X, Bradshaw D, Shine R. Capital versus income breeding: An ectothermic perspective. Oikos. 1998;83:333.Article 

Google Scholar 
72.de Mazancourt C, Schwartz MW. Starve a competitor: evolution of luxury consumption as a competitive strategy. Theor Ecol. 2012;13:37–49.Article 

Google Scholar 
73.Ejsmond MJ, Varpe Ø, Czarnoleski M, Kozłowski J. Seasonality in offspring value and trade-offs with growth explain capital breeding. Am Nat. 2015;186:E111–25.Article 

Google Scholar 
74.Kourmentza C, Plácido J, Venetsaneas N, Burniol-Figols A, Varrone C, Gavala HN, et al. Recent advances and challenges towards sustainable polyhydroxyalkanoate (PHA) production. Bioengineering. 2017;4:55.PubMed Central 
Article 
CAS 
PubMed 

Google Scholar 
75.Wilson WA, Roach PJ, Montero M, Baroja-Fernández E, Muñoz FJ, Eydallin G, et al. Regulation of glycogen metabolism in yeast and bacteria. FEMS Microbiol Rev. 2010;34:952–85.CAS 
PubMed 
Article 

Google Scholar 
76.Doi Y, Kawaguchi Y, Koyama N, Nakamura S, Hiramitsu M, Yoshida Y, et al. Synthesis and degradation of polyhydroxyalkanoates in Alcaligenes eutrophus. FEMS Microbiol Lett. 1992;103:103–8.CAS 
Article 

Google Scholar 
77.Alvarez AHM, Kalscheuer R, Steinbüchel A. Accumulation of storage lipids in species of Rhodococcus and Nocardia and effect of inhibitors and polyethylene glycol. Lipid. 1997;99:239–46.CAS 
Article 

Google Scholar 
78.Parrou JL, Enjalbert B, Plourde L, Bauche A, Gonzalez B, François J. Dynamic responses of reserve carbohydrate metabolism under carbon and nitrogen limitations in Saccharomyces cerevisiae. Yeast. 1999;15:191–203.CAS 
PubMed 
Article 

Google Scholar 
79.Gebremariam SY, Beutel MW, Christian D, Hess TF. Research advances and challenges in the microbiology of enhanced biological phosphorus removal-A critical review. Water Environ Res. 2011;83:195–219.CAS 
PubMed 
Article 

Google Scholar 
80.Ratledge C. Fatty acid biosynthesis in microorganisms being used for single cell oil production. Biochimie. 2004;86:807–15.CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
81.Matin A, Veldhuis C, Stegeman V, Veenhuis M. Selective advantage of a Spirillum sp. in a carbon-limited environment. Accumulation of poly-β-hydroxybutyric acid and its role in starvation. J Gen Microbiol. 1979;112:349–55.CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
82.Poblete-Castro I, Escapa IF, Jäger C, Puchalka J, Chi Lam C, Schomburg D, et al. The metabolic response of P. putida KT2442 producing high levels of polyhydroxyalkanoate under single- and multiple-nutrient-limited growth: Highlights from a multi-level omics approach. Micro Cell Fact. 2012;11:34.CAS 
Article 

Google Scholar 
83.Wilkinson JF, Munro ALS. The influence of growth limiting conditions on the synthesis of possible carbon and energy storage polymers in Bacillus megaterium. In: Powell EO, Evans CGT, Strange RE, Tempest DW, editors. Microbial physiology and continuous culture, Proceedings of the Third International Symposium. Salisbury, United Kingdom: Her Majesty’s Stationery Office; 1967. p. 173–85.84.Alvarez HM, Mayer F, Fabritius D, Steinbüchel A. Formation of intracytoplasmic lipid inclusions by Rhodococcus opacus strain PD630. Arch Microbiol. 1996;165:377–86.CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
85.Orchard ED, Benitez-Nelson CR, Pellechia PJ, Lomas MW, Dyhrman ST. Polyphosphate in Trichodesmium from the low-phosphorus Sargasso Sea. Limnol Oceanogr. 2010;55:2161–9.CAS 
Article 

Google Scholar 
86.Li J, Mara P, Schubotz F, Sylvan JB, Burgaud G, Klein F, et al. Recycling and metabolic flexibility dictate life in the lower oceanic crust. Nature. 2020;579:250–5.CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
87.Preiss J, Romeo T. Molecular biology and regulatory aspects of glycogen biosynthesis in bacteria. Prog Nucleic Acid Res Mol Biol. 1994;47:299–329.CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
88.Mackerras AH, de Chazal NM, Smith GD. Transient accumulations of cyanophycin in Anabaena cylindrica and Synechocystis 6308. J Gen Microbiol. 1990;136:2057–65.CAS 
Article 

Google Scholar 
89.Parnas H, Cohen D. The optimal strategy for the metabolism of reserve materials in micro-organisms. J Theor Biol. 1976;56:19–55.CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
90.Dijkstra P, Salpas E, Fairbanks D, Miller EB, Hagerty SB, van Groenigen KJ, et al. High carbon use efficiency in soil microbial communities is related to balanced growth, not storage compound synthesis. Soil Biol Biochem. 2015;89:35–43.CAS 
Article 

Google Scholar 
91.Empadinhas N, da Costa MS. Osmoadaptation mechanisms in prokaryotes: distribution of compatible solutes. Int Microbiol. 2008;11:151–61.CAS 
PubMed 
PubMed Central 

Google Scholar 
92.Albi T, Serrano A. Inorganic polyphosphate in the microbial world. Emerging roles for a multifaceted biopolymer. World J Microbiol Biotechnol. 2016;32:27.PubMed 
Article 
CAS 
PubMed Central 

Google Scholar 
93.Sekar K, Linker SM, Nguyen J, Grünhagen A, Stocker R, Sauer U. Bacterial glycogen provides short-term benefits in changing environments. Appl Environ Microbiol. 2020;86:e00049–20.CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
94.Silljé HH, Paalman JW, ter Schure EG, Olsthoorn SQ, Verkleij AJ, Boonstra J, et al. Function of trehalose and glycogen in cell cycle progression and cell viability in Saccharomyces cerevisiae. J Bacteriol. 1999;181:396–400.PubMed 
PubMed Central 
Article 

Google Scholar 
95.Jahid IK, Silva AJ, Benitez JA. Polyphosphate stores enhance the ability of Vibrio cholerae to overcome environmental stresses in a low-phosphate environment. Appl Environ Microbiol. 2006;72:7043–9.CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
96.Ramírez-Trujillo JA, Dunn MF, Suárez-Rodríguez R, Hernández-Lucas I. The Sinorhizobium meliloti glyoxylate cycle enzyme isocitrate lyase (AceA) is required for the utilization of poly-β-hydroxybutyrate during carbon starvation. Ann Microbiol. 2016;66:921–4.Article 
CAS 

Google Scholar 
97.Vagabov VM, Trilisenko LV, Kulaev IS. Dependence of inorganic polyphosphate chain length on the orthophosphate content in the culture medium of the yeast Saccharomyces cerevisiae. Biochemistry. 2000;65:6.
Google Scholar 
98.Schimz K-L, Irrgang K, Overhoff B. Glycogen, a cytoplasmic reserve polysaccharide of Cellulomonas sp. (DSM20108): Its identification, carbon source-dependent accumulation, and degradation during starvation. FEMS Microbiol Lett. 1985;30:165–9.CAS 
Article 

Google Scholar 
99.Kalscheuer R, Stöveken T, Malkus U, Reichelt R, Golyshin PN, Sabirova JS, et al. Analysis of storage lipid accumulation in Alcanivorax borkumensis: Evidence for alternative triacylglycerol biosynthesis routes in bacteria. J Bacteriol. 2007;189:918–28.CAS 
PubMed 
Article 

Google Scholar 
100.Busuioc M, Mackiewicz K, Buttaro BA, Piggot PJ. Role of intracellular polysaccharide in persistence of Streptococcus mutans. J Bacteriol. 2009;191:7315–22.CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
101.Ruiz JA, Lopez NI, Fernandez RO, Mendez BS. Polyhydroxyalkanoate degradation Is associated with nucleotide accumulation and enhances stress resistance and survival of Pseudomonas oleovorans in natural water microcosms. Appl Environ Microbiol. 2001;67:225–30.CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
102.Klotz A, Georg J, Bučinská L, Watanabe S, Reimann V, Januszewski W, et al. Awakening of a dormant cyanobacterium from nitrogen chlorosis reveals a genetically determined program. Curr Biol. 2016;26:2862–72.CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
103.Elbein AD. New insights on trehalose: a multifunctional molecule. Glycobiology. 2003;13:17R–27R.CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
104.Obruca S, Sedlacek P, Koller M. The underexplored role of diverse stress factors in microbial biopolymer synthesis. Bioresour Technol. 2021;326:124767.CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
105.Ayub ND, Tribelli PM, López NI. Polyhydroxyalkanoates are essential for maintenance of redox state in the Antarctic bacterium Pseudomonas sp. 14-3 during low temperature adaptation. Extremophiles. 2009;13:59–66.CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
106.Grime JP. Evidence for the existence of three primary strategies in plants and its relevance to ecological and evolutionary theory. Am Nat. 1977;111:1169–94.Article 

Google Scholar 
107.Ho A, Kerckhof F-M, Luke C, Reim A, Krause S, Boon N, et al. Conceptualizing functional traits and ecological characteristics of methane-oxidizing bacteria as life strategies: Functional traits of methane-oxidizing bacteria. Environ Microbiol Rep. 2013;5:335–45.CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
108.Santillan E, Seshan H, Constancias F, Wuertz S. Trait‐based life‐history strategies explain succession scenario for complex bacterial communities under varying disturbance. Environ Microbiol. 2019;21:3751–64.CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
109.Chesson P. Mechanisms of maintenance of species diversity. Annu Rev Ecol Syst. 2000;31:343–66.Article 

Google Scholar 
110.Loreau M, de Mazancourt C. Biodiversity and ecosystem stability: a synthesis of underlying mechanisms. Ecol Lett. 2013;16:106–15.PubMed 
Article 
PubMed Central 

Google Scholar 
111.Geyer KM, Kyker-Snowman E, Grandy AS, Frey SD. Microbial carbon use efficiency: accounting for population, community, and ecosystem-scale controls over the fate of metabolized organic matter. Biogeochemistry. 2016;127:173–88.CAS 
Article 

Google Scholar 
112.Manzoni S, Porporato A. Soil carbon and nitrogen mineralization: Theory and models across scales. Soil Biol Biochem. 2009;41:1355–79.CAS 
Article 

Google Scholar 
113.Schultz P, Urban NR. Effects of bacterial dynamics on organic matter decomposition and nutrient release from sediments: a modeling study. Ecol Model. 2008;210:1–14.CAS 
Article 

Google Scholar 
114.Torres-Dorante LO, Claassen N, Steingrobe B, Olfs H-W. Polyphosphate determination in calcium acetate-lactate (CAL) extracts by an indirect colorimetric method. J Plant Nutr Soil Sci. 2004;167:701–3.CAS 
Article 

Google Scholar 
115.Micić V, Köster J, Kruge MA, Engelen B, Hofmann T. Bacterial wax esters in recent fluvial sediments. Org Geochem. 2015;89–90:44–55.Article 
CAS 

Google Scholar 
116.Mooshammer M, Wanek W, Zechmeister-Boltenstern S, Richter A. Stoichiometric imbalances between terrestrial decomposer communities and their resources: mechanisms and implications of microbial adaptations to their resources. Front Microbiol 2014;5:1–10.Article 

Google Scholar 
117.Op De Beeck M, Troein C, Siregar S, Gentile L, Abbondanza G, Peterson C, et al. Regulation of fungal decomposition at single-cell level. ISME J. 2020;14:896–905.PubMed 
PubMed Central 
Article 

Google Scholar 
118.Liang C, Amelung W, Lehmann J, Kästner M. Quantitative assessment of microbial necromass contribution to soil organic matter. Glob Chang Biol. 2019;25:3578–90.PubMed 
Article 
PubMed Central 

Google Scholar 
119.Ducklow H, Steinberg D, Buesseler K. Upper ocean carbon export and the biological pump. Oceanography. 2001;14:50–8.Article 

Google Scholar 
120.Wieder WR, Allison SD, Davidson EA, Georgiou K, Hararuk O, He Y, et al. Explicitly representing soil microbial processes in Earth system models: Soil microbes in Earth system models. Glob Biogeochem Cycles. 2015;29:1782–800.CAS 
Article 

Google Scholar 
121.Schimel J, Weintraub MN. The implications of exoenzyme activity on microbial carbon and nitrogen limitation in soil: a theoretical model. Soil Biol Biochem. 2003;35:549–63.CAS 
Article 

Google Scholar 
122.Ni B-J, Fang F, Rittmann BE, Yu H-Q. Modeling microbial products in activated sludge under feast-famine conditions. Environ Sci Technol. 2009;43:2489–97.CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
123.Godwin CM, Cotner JB. Stoichiometric flexibility in diverse aquatic heterotrophic bacteria is coupled to differences in cellular phosphorus quotas. Front Microbiol 2015;6:1–15.Article 

Google Scholar 
124.Camenzind T, Philipp Grenz K, Lehmann J, Rillig MC. Soil fungal mycelia have unexpectedly flexible stoichiometric C:N and C:P ratios. Ecol Lett. 2021;24:208–18.PubMed 
Article 
PubMed Central 

Google Scholar 
125.Fatichi S, Manzoni S, Or D, Paschalis A. A mechanistic model of microbially mediated soil biogeochemical processes: a reality check. Glob Biogeochem Cycles. 2019;33:620–48.CAS 
Article 

Google Scholar 
126.Sistla SA, Rastetter EB, Schimel JP. Responses of a tundra system to warming using SCAMPS: a stoichiometrically coupled, acclimating microbe–plant–soil model. Ecol Monogr. 2014;84:151–70.Article 

Google Scholar 
127.Lashermes G, Gainvors-Claisse A, Recous S, Bertrand I. Enzymatic strategies and carbon use efficiency of a litter-decomposing fungus grown on maize leaves, stems, and roots. Front Microbiol 2016;7:1–14.Article 

Google Scholar 
128.Lee ZM, Schmidt TM. Bacterial growth efficiency varies in soils under different land management practices. Soil Biol Biochem. 2014;69:282–90.CAS 
Article 

Google Scholar 
129.Camenzind T, Lehmann A, Ahland J, Rumpel S, Rillig MC. Trait‐based approaches reveal fungal adaptations to nutrient‐limiting conditions. Environ Microbiol. 2020;22:3548–60.CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
130.Manzoni S, Čapek P, Mooshammer M, Lindahl BD, Richter A, Šantrůčková H. Optimal metabolic regulation along resource stoichiometry gradients. Ecol Lett. 2017;20:1182–91.PubMed 
Article 
PubMed Central 

Google Scholar 
131.Tang J, Riley WJ. Weaker soil carbon–climate feedbacks resulting from microbial and abiotic interactions. Nat Clim Chang. 2015;5:5.CAS 
Article 

Google Scholar 
132.Lee KS, Pereira FC, Palatinszky M, Behrendt L, Alcolombri U, Berry D, et al. Optofluidic Raman-activated cell sorting for targeted genome retrieval or cultivation of microbial cells with specific functions. Nat Protoc. 2021;16:634–76.CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
133.Günther S, Trutnau M, Kleinsteuber S, Hause G, Bley T, Röske I, et al. Dynamics of polyphosphate-accumulating bacteria in wastewater treatment plant microbial communities detected via DAPI (4′,6′-diamidino-2-phenylindole) and tetracycline labeling. Appl Environ Microbiol. 2009;75:2111–21.PubMed 
PubMed Central 
Article 
CAS 

Google Scholar 
134.Singleton CM, Petriglieri F, Kristensen JM, Kirkegaard RH, Michaelsen TY, Andersen MH, et al. Connecting structure to function with the recovery of over 1000 high-quality metagenome-assembled genomes from activated sludge using long-read sequencing. Nat Commun. 2021;12:2009.CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
135.Link H, Fuhrer T, Gerosa L, Zamboni N, Sauer U. Real-time metabolome profiling of the metabolic switch between starvation and growth. Nat Methods. 2015;12:1091–7.CAS 
PubMed 
Article 

Google Scholar 
136.Warren CR. Altitudinal transects reveal large differences in intact lipid composition among soils. Soil Res. 2021;59:644–59.CAS 
Article 

Google Scholar 
137.Wilkinson J. The problem of energy-storage compounds in bacteria. Exp Cell Res. 1959;7:111–30.Article 

Google Scholar 
138.Nickels JS, King JD, White DC. Poly-β-hydroxybutyrate accumulation as a measure of unbalanced growth of the estuarine detrital microbiota. Appl Environ Microbiol. 1979;37:459–65.CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
139.Murphy DJ. The dynamic roles of intracellular lipid droplets: from archaea to mammals. Protoplasma. 2012;249:541–85.CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
140.Alvarez HM. Triacylglycerol and wax ester-accumulating machinery in prokaryotes. Biochimie. 2016;120:28–39.CAS 
PubMed 
Article 

Google Scholar 
141.Koller M, Maršálek L, de Sousa Dias MM, Braunegg G. Producing microbial polyhydroxyalkanoate (PHA) biopolyesters in a sustainable manner. N Biotechnol. 2017;37:24–38.CAS 
PubMed 
Article 

Google Scholar 
142.Obruca S, Sedlacek P, Slaninova E, Fritz I, Daffert C, Meixner K, et al. Novel unexpected functions of PHA granules. Appl Microbiol Biotechnol. 2020;104:4795–810.CAS 
PubMed 
Article 

Google Scholar 
143.Roach PJ, Depaoli-Roach AA, Hurley TD, Tagliabracci VS. Glycogen and its metabolism: some new developments and old themes. Biochem J. 2012;441:763–87.CAS 
PubMed 
Article 

Google Scholar 
144.Wang L, Wang M, Wise MJ, Liu Q, Yang T, Zhu Z, et al. Recent progress in the structure of glycogen serving as a durable energy reserve in bacteria. World J Microbiol Biotechnol. 2020;36:14.PubMed 
Article 

Google Scholar 
145.Ruhal R, Kataria R, Choudhury B. Trends in bacterial trehalose metabolism and significant nodes of metabolic pathway in the direction of trehalose accumulation: Trehalose metabolism in bacteria. Micro Biotechnol. 2013;6:493–502.Article 
CAS 

Google Scholar 
146.Kalscheuer R. Genetics of wax ester and triacylglycerol biosynthesis in bacteria. In: Timmis KN, editor. Handbook of hydrocarbon and lipid microbiology. Berlin, Heidelberg: Springer Berlin Heidelberg; 2010. p. 527–35.147.Rao NN, Gómez-García MR, Kornberg A. Inorganic polyphosphate: essential for growth and survival. Annu Rev Biochem. 2009;78:605–47.CAS 
PubMed 
Article 

Google Scholar 
148.Denoncourt A, Downey M. Model systems for studying polyphosphate biology: a focus on microorganisms. Curr Genet. 2021;67:331–46.CAS 
PubMed 
Article 

Google Scholar 
149.Füser G, Steinbüchel A. Analysis of genome sequences for genes of cyanophycin metabolism: Identifying putative cyanophycin metabolizing prokaryotes. Macromol Biosci. 2007;7:278–96.PubMed 
Article 
CAS 
PubMed Central 

Google Scholar 
150.Watzer B, Forchhammer K. Cyanophycin: a nitrogen-rich reserve polymer. In: Tiwari A, editor. Cyanobacteria. London: InTech; 2018. More

1.Leach JE, Tringe SG. Plant–microbiome interactions: from community assembly to plant health. Nat Rev Microbiol. 2020;18:607–21.PubMed 
Article 
CAS 
PubMed Central 

Google Scholar 
2.Pii Y, Mimmo T, Tomasi N, Terzano R, Cesco S, Crecchio C. Microbial interactions in the rhizosphere: beneficial influences of plant growth-promoting rhizobacteria on nutrient acquisition process. A Rev Biol Fertil Soils. 2015;51:403–21.CAS 
Article 

Google Scholar 
3.Backer R, Rokem JS, Ilangumaran G, Lamont J, Praslickova D, Ricci E, et al. Plant growth-promoting rhizobacteria: context, mechanisms of action, and roadmap to commercialization of biostimulants for sustainable agriculture. Front Plant Sci. 2018;871:1473–89.Article 

Google Scholar 
4.Lugtenberg B, Kamilova F. Plant-growth-promoting rhizobacteria. Annu Rev Microbiol. 2009;63:541–56.CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
5.Bhattacharyya PN, Jha DK. Plant growth-promoting rhizobacteria (PGPR): emergence in agriculture. World J Microbiol Biotechnol. 2012;28:1327–50.CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
6.Leach JE, Triplett LR, Argueso CT, Trivedi P. Communication in the phytobiome. Cell. 2017;169:587–96.CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
7.Vorholt JA, Vogel C, Carlström CI, Müller DB. Establishing causality: opportunities of synthetic communities for plant microbiome research. Cell Host Microbe. 2017;22:142–55.CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
8.Douglas AE. The microbial exometabolome: ecological resource and architect of microbial communities. PTRBAE. 2020;375:20190250.CAS 
PubMed 
PubMed Central 

Google Scholar 
9.Turroni F, Milani C, Duranti S, Mahony J, van Sinderen D, Ventura M. Glycan utilization and cross-feeding activities by Bifidobacteria. Trends Microbiol. 2018;26:339–50.CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
10.Evans CR, Kempes CP, Price-Whelan A, Dietrich LEP. Metabolic heterogeneity and cross-feeding in bacterial multicellular systems. Trends Microbiol. 2020;28:732–43.CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
11.Smith NW, Shorten PR, Altermann E, Roy NC, McNabb WC. The classification and evolution of bacterial cross-feeding. Front Ecol Evol. 2019;7:153.Article 

Google Scholar 
12.Santoyo G, del Orozco-Mosqueda MC, Govindappa M. Mechanisms of biocontrol and plant growth-promoting activity in soil bacterial species of Bacillus and Pseudomonas: a review. Biocontrol Sci Technol. 2012;22:855–72.Article 

Google Scholar 
13.Borriss R. Use of plant-associated Bacillus strains as biofertilizers and biocontrol agents in agriculture. Bacteria in agrobiology: plant growth responses. Springer: Berlin; 2011. 41–76.14.Xiong W, Guo S, Jousset A, Zhao Q, Wu H, Li R, et al. Bio-fertilizer application induces soil suppressiveness against Fusarium wilt disease by reshaping the soil microbiome. Soil Biol Biochem. 2017;114:238–47.CAS 
Article 

Google Scholar 
15.Qin Y, Shang Q, Zhang Y, Li P, Chai Y. Bacillus amyloliquefaciens L-S60 reforms the rhizosphere bacterial community and improves growth conditions in cucumber plug seedling. Front Microbiol. 2017;8:2620.PubMed 
PubMed Central 
Article 

Google Scholar 
16.Compant S, Samad A, Faist H, Sessitsch A. A review on the plant microbiome: ecology, functions, and emerging trends in microbial application. J Adv Res. 2019;19:29–37.CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
17.Cao Y, Zhang Z, Ling N, Yuan Y, Zheng X, Shen B, et al. Bacillus subtilis SQR9 can control Fusarium wilt in cucumber by colonizing plant roots. Biol Fertil Soils. 2011;47:495–506.CAS 
Article 

Google Scholar 
18.Xu Z, Shao J, Li B, Yan X, Shen Q, Zhang R. Contribution of bacillomycin D in Bacillus amyloliquefaciens SQR9 to antifungal activity and biofilm formation. Appl Environ Microbiol. 2013;79:808–15.CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
19.Chen L, Liu Y, Wu G, Veronican Njeri K, Shen Q, Zhang N, et al. Induced maize salt tolerance by rhizosphere inoculation of Bacillus amyloliquefaciens SQR9. Physiol plant. 2016;158:34–44.CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
20.Blake C, Nordgaard Christensen M, Kovács ÁT. Molecular aspects of plant growth promotion and protection by Bacillus subtilis. Mol Plant Microbe Interact. 2020;34:15–25.PubMed 
Article 
PubMed Central 

Google Scholar 
21.Al-Ali A, Deravel J, Krier F, Béchet M, Ongena M, Jacques P. Biofilm formation is determinant in tomato rhizosphere colonization by Bacillus velezensis FZB42. Environ Sci Pollut Res. 2018;25:29910–20.CAS 
Article 

Google Scholar 
22.Xu Z, Mandic-Mulec I, Zhang H, Liu Y, Sun X, Feng H, et al. Antibiotic bacillomycin D affects iron acquisition and biofilm formation in Bacillus velezensis through a Btr-mediated FeuABC-dependent pathway. Cel Rep. 2019;29:1192–202.CAS 
Article 

Google Scholar 
23.Murashige T, Skoog F. A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol Plant. 1962;15:473–97.CAS 
Article 

Google Scholar 
24.Bai Y, Müller DB, Srinivas G, Garrido-Oter R, Potthoff E, Rott M, et al. Functional overlap of the Arabidopsis leaf and root microbiota. Nature. 2015;528:364–9.CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
25.Zhou C, Shi L, Ye B, Feng H, Zhang J, Zhang R, et al. pheS *, an effective host-genotype-independent counter-selectable marker for marker-free chromosome deletion in Bacillus amyloliquefaciens. Appl Microbiol Biotechnol. 2017;101:217–27.CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
26.Feng H, Zhang N, Fu R, Liu Y, Krell T, Du W, et al. Recognition of dominant attractants by key chemoreceptors mediates recruitment of plant growth-promoting rhizobacteria. Environ Microbiol. 2019;21:402–15.CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
27.Lambertsen L, Sternberg C, Molin S. Mini-Tn7 transposons for site-specific tagging of bacteria with fluorescent proteins. Environ Microbiol. 2004;6:726–32.CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
28.Seemann T. Prokka: rapid prokaryotic genome annotation. Bioinformatics. 2014;30:2068–9.CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
29.Machado D, Andrejev S, Tramontano M, Patil KR. Fast automated reconstruction of genome-scale metabolic models for microbial species and communities. Nucleic Acids Res. 2018;46:7542–53.CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
30.Lieven C, Beber ME, Olivier BG, Bergmann FT, Ataman M, Babaei P, et al. MEMOTE for standardized genome-scale metabolic model testing. Nat Biotechnol. 2020;38:272–6.CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
31.Zelezniak A, Andrejev S, Ponomarova O, Mende DR, Bork P, Patil KR. Metabolic dependencies drive species co-occurrence in diverse microbial communities. Proc Natl Acad Sci USA. 2015;112:6449–54.CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
32.Edgar RC. UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods. 2013;10:996–8.CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
33.Parks DH, Tyson GW, Hugenholtz P, Beiko RG. STAMP: statistical analysis of taxonomic and functional profiles. Bioinformatics. 2014;30:3123–4.CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
34.Branda SS, González-Pastor JE, Ben-Yehuda S, Losick R, Kolter R. Fruiting body formation by Bacillus subtilis. Proc Natl Acad Sci USA. 2001;98:11621–6.CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
35.Page AJ, Cummins CA, Hunt M, Wong VK, Reuter S, Holden MTG, et al. Roary: rapid large-scale prokaryote pan genome analysis. Bioinformatics. 2015;31:3691–3.CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
36.Langdon WB. Performance of genetic programming optimised Bowtie2 on genome comparison and analytic testing (GCAT) benchmarks. BioData Min. 2015;8:1–7.CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
37.Love MI, Huber W, Anders S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 2014;15:1–21.Article 
CAS 

Google Scholar 
38.Huerta-Cepas J, Forslund K, Coelho LP, Szklarczyk D, Jensen LJ, von Mering C, et al. Fast genome-wide functional annotation through orthology assignment by eggNOG-mapper. Mol Biol Evol. 2017;34:2115–22.CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
39.Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔ C(T) method. Methods. 2001;25:402–8.CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
40.Ling N, Raza W, Ma J, Huang Q, Shen Q. Identification and role of organic acids in watermelon root exudates for recruiting Paenibacillus polymyxa SQR-21 in the rhizosphere. Eur J Soil Biol. 2011;47:374–9.CAS 
Article 

Google Scholar 
41.Gordillo F, Chávez FP, Jerez CA. Motility and chemotaxis of Pseudomonas sp. B4 towards polychlorobiphenyls and chlorobenzoates. FEMS Microbiol Ecol. 2007;60:322–8.CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
42.Dragoš A, Kiesewalter H, Martin M, Hsu CY, Hartmann R, Wechsler T, et al. Division of labor during biofilm matrix production. Curr Biol. 2018;28:1903–.e5.PubMed 
PubMed Central 
Article 
CAS 

Google Scholar 
43.Ahmad F, Ahmad I, Khan MS. Screening of free-living rhizospheric bacteria for their multiple plant growth promoting activities. Microbiol Res. 2008;163:173–81.CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
44.Lynne AM, Haarmann D, Louden BC. Use of blue agar CAS assay for siderophore detection. J Microbiol Biol Educ. 2011;12:51–53.PubMed 
PubMed Central 
Article 

Google Scholar 
45.Nautiyal CS. An efficient microbiological growth medium for screening phosphate solubilizing microorganisms. FEMS Microbiol Lett. 1999;170:265–70.CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
46.Ansari FA, Ahmad I. Fluorescent Pseudomonas -FAP2 and Bacillus licheniformis interact positively in biofilm mode enhancing plant growth and photosynthetic attributes. Sci Rep. 2019;9:1–12.
Google Scholar 
47.Santhanam R, Menezes RC, Grabe V, Li D, Baldwin IT, Groten K. A suite of complementary biocontrol traits allows a native consortium of root‐associated bacteria to protect their host plant from a fungal sudden‐wilt disease. Mol Ecol. 2019;28:1154–69.CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
48.Santhanam R, Luu VT, Weinhold A, Goldberg J, Oh Y, Baldwin IT. Native root-associated bacteria rescue a plant from a sudden-wilt disease that emerged during continuous cropping. Proc Natl Acad Sci USA. 2015;112:E5013–E5120.CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
49.Berendsen RL, Vismans G, Yu K, Song Y, de Jonge R, Burgman WP, et al. Disease-induced assemblage of a plant-beneficial bacterial consortium. ISME J. 2018;12:1496–507.CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
50.Ren D, Madsen JS, Sørensen SJ, Burmølle M. High prevalence of biofilm synergy among bacterial soil isolates in cocultures indicates bacterial interspecific cooperation. ISME J. 2015;9:81–89.CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
51.Oliveira NM, Martinez-Garcia E, Xavier J, Durham WM, Kolter R, Kim W, et al. Biofilm formation as a response to ecological competition. PLoS Biol. 2015;13:1–23.
Google Scholar 
52.Gallegos-Monterrosa R, Mhatre E, Kovács ÁT. Specific Bacillus subtilis 168 variants form biofilms on nutrient-rich medium. Microbiology. 2016;162:1922–32.CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
53.Shao J, Xu Z, Zhang N, Shen Q, Zhang R. Contribution of indole-3-acetic acid in the plant growth promotion by the rhizospheric strain Bacillus amyloliquefaciens SQR9. Biol Fertil Soils. 2015;51:321–30.CAS 
Article 

Google Scholar 
54.Stopnisek N, Shade A. Persistent microbiome members in the common bean rhizosphere: an integrated analysis of space, time, and plant genotype. ISME J. 2021;15:2708–22.PubMed 
PubMed Central 
Article 

Google Scholar 
55.Sivasakthi S, Usharani G, Saranraj P. Biocontrol potentiality of plant growth promoting bacteria (PGPR)—Pseudomonas fluorescens and Bacillus subtilis: a review. Afr J Agric Res. 2014;9:1265–77.
Google Scholar 
56.Dardanelli MS, Manyani H, González-Barroso S, Rodríguez-Carvajal MA, Gil-Serrano AM, Espuny MR, et al. Effect of the presence of the plant growth promoting rhizobacterium (PGPR) Chryseobacterium balustinum Aur9 and salt stress in the pattern of flavonoids exuded by soybean roots. Plant Soil. 2010;328:483–93.CAS 
Article 

Google Scholar 
57.Gómez Expósito R, Postma J, Raaijmakers JM, de Bruijn I. Diversity and activity of Lysobacter species from disease suppressive soils. Front Microbiol. 2015;6:1243.PubMed 
PubMed Central 
Article 

Google Scholar 
58.Han Q, Ma Q, Chen Y, Tian B, Xu L, Bai Y, et al. Variation in rhizosphere microbial communities and its association with the symbiotic efficiency of rhizobia in soybean. ISME J. 2020;14:1915–28.CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
59.Peterson SB, Dunn AK, Klimowicz AK, Handelsman J. Peptidoglycan from Bacillus cereus mediates commensalism with rhizosphere bacteria from the Cytophaga-Flavobacterium group. Appl Environ Microbiol. 2006;72:5421–7.CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
60.Tao C, Li R, Xiong W, Shen Z, Liu S, Wang B, et al. Bio-organic fertilizers stimulate indigenous soil Pseudomonas populations to enhance plant disease suppression. Microbiome. 2020;8:137.PubMed 
PubMed Central 
Article 

Google Scholar 
61.Kumar A, Singh J. Biofilms forming microbes: diversity and potential application in plant-microbe interaction and plant growth. Springer: Cham; 2020. 173−97.62.Tabassum B, Khan A, Tariq M, Ramzan M, Iqbal Khan MS, Shahid N, et al. Bottlenecks in commercialisation and future prospects of PGPR. Appl Soil Ecol. 2017;121:102–17.Article 

Google Scholar 
63.Madsen JS, Røder HL, Russel J, Sørensen H, Burmølle M, Sørensen SJ. Coexistence facilitates interspecific biofilm formation in complex microbial communities. Environ Microbiol. 2016;18:2565–74.CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
64.Burmølle M, Webb JS, Rao D, Hansen LH, Sørensen SJ, Kjelleberg S. Enhanced biofilm formation and increased resistance to antimicrobial agents and bacterial invasion are caused by synergistic interactions in multispecies biofilms. Appl Environ Microbiol. 2006;72:3916–23.PubMed 
PubMed Central 
Article 
CAS 

Google Scholar 
65.Lee KWK, Periasamy S, Mukherjee M, Xie C, Kjelleberg S, Rice SA. Biofilm development and enhanced stress resistance of a model, mixed-species community biofilm. ISME J. 2014;8:894–907.CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
66.Yannarell SM, Grandchamp GM, Chen SY, Daniels KE, Shank EA. A dual-species biofilm with emergent mechanical and protective properties. J Bacteriol. 2019;201:e00670–18.CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
67.Preussger D, Giri S, Muhsal LK, Oña L, Kost C. Reciprocal fitness feedbacks promote the evolution of mutualistic cooperation. Curr Biol. 2020;30:1–11.Article 
CAS 

Google Scholar 
68.Nadell CD, Drescher K, Foster KR. Spatial structure, cooperation, and competition in biofilms. Nat Rev Microbiol. 2016;14:589–600.CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
69.Estrela S, Sanchez-Gorostiaga A, Vila JCC, Sanchez A. Nutrient dominance governs the assembly of microbial communities in mixed nutrient environments. eLife. 2021;10:e65948.PubMed 
PubMed Central 
Article 

Google Scholar 
70.Molina-Santiago C, Pearson JR, Navarro Y, Berlanga-Clavero MV, Caraballo-Rodriguez AM, Petras D, et al. The extracellular matrix protects Bacillus subtilis colonies from Pseudomonas invasion and modulates plant co-colonization. Nat Commun. 2019;10:1919.PubMed 
PubMed Central 
Article 
CAS 

Google Scholar 
71.Yan Q, Lopes LD, Shaffer BT, Kidarsa TA, Vining O, Philmus B, et al. Secondary metabolism and interspecific competition affect accumulation of spontaneous mutants in the GacS-GacA regulatory system in Pseudomonas protegens. mBio. 2018;9:e01845–17.CAS 
PubMed 
PubMed Central 

Google Scholar 
72.Mee MT, Collins JJ, Church GM, Wang HH. Syntrophic exchange in synthetic microbial communities. Proc Natl Acad Sci USA. 2014;111:E2149–E2156.CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
73.D’Souza G, Shitut S, Preussger D, Yousif G, Waschina S, Kost C. Ecology and evolution of metabolic cross-feeding interactions in bacteria. Nat Prod Rep. 2018;35:455–88.PubMed 
Article 
PubMed Central 

Google Scholar 
74.Goldford JE, Lu N, Bajić D, Estrela S, Tikhonov M, Sanchez-Gorostiaga A, et al. Emergent simplicity in microbial community assembly. Science. 2018;361:469–74.CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
75.Lawrence D, Fiegna F, Behrends V, Bundy JG, Phillimore AB, Bell T, et al. Species interactions alter evolutionary responses to a novel environment. PLoS Biol. 2012;10:e1001330.CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
76.Evans R, Beckerman AP, Wright RCT, McQueen-Mason S, Bruce NC, Brockhurst MA. Eco-evolutionary dynamics set the tempo and trajectory of metabolic evolution in multispecies communities. Curr Biol. 2020;30:1–5.Article 
CAS 

Google Scholar 
77.Gamez RM, Ramirez S, Montes M, Cardinale M. Complementary dynamics of banana root colonization by the plant growth-promoting rhizobacteria Bacillus amyloliquefaciens Bs006 and Pseudomonas palleroniana Ps006 at spatial and temporal scales. Micro Ecol. 2020;80:656–68.CAS 
Article 

Google Scholar 
78.Feng H, Zhang N, Fu R, Liu Y, Krell T, Du W, et al. Recognition of dominant attractants by key chemoreceptors mediates recruitment of plant growth-promoting rhizobacteria. Environ Microbiol. 2019;21:402–15.CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
79.Feng H, Zhang N, Du W, Zhang H, Liu Y, Fu R, et al. Identification of chemotaxis compounds in root exudates and their sensing chemoreceptors in plant-growth-promoting rhizobacteria Bacillus amyloliquefaciens SQR9. Mol Plant Microbe interact. 2018;31:995–1005.CAS 
PubMed 
Article 

Google Scholar 
80.Xu Z, Xie J, Zhang H, Wang D, Shen Q, Zhang R. Enhanced control of plant wilt disease by a xylose-inducible degQ gene engineered into Bacillus velezensis strain SQR9XYQ. Phytopathology. 2019;109:36–43.CAS 
PubMed 
Article 
PubMed Central 

Google Scholar  More

1.Kang CS, Liang X, Dershwitz P, Gu W, Schepers A, Flatley A, et al. Evidence for methanobactin “theft” and novel chalkophore production in methanotrophs: impact on methanotrophic-mediated methylmercury degradation. ISME J. 2021;https://doi.org/10.1038/s41396-021-01062-1.2.Semrau JD, DiSpirito AA, Obulisamy PK, Kang-Yun CS. Methanobactin from methanotrophs: genetics, structure, function and potential applications. FEMS Microbiol Lett. 2020;367:fnaa045.CAS 
Article 

Google Scholar 
3.Kim HJ, Graham DW, DiSpiito AA, Alterman MA, Galeva N, Larive CK, et al. Methanobactin: a copper-acquisition compound from methane-oxidizing bacteria. Science. 2004;305:1612–5.CAS 
Article 

Google Scholar 
4.Lu X, Gu W, Zhao L, Farhan Ul Haque M, DiSpirito AA, Semrau JD, et al. Methylmercury uptake and degradation by methanotrophs. Sci Adv. 2017;3:e1700041.Article 

Google Scholar 
5.Ve T, Mathisen K, Helland R, Karlsen OA, Fjellbirkeland A, Røhr ÅK, et al. The Methylococcus capsulatus (Bath) secreted protein, MopE*, binds both reduced and oxidized copper. PLoS ONE. 2012;7:e43146.CAS 
Article 

Google Scholar 
6.DiSpirito AA, Semrau JD, Murrell JC, Gallagher WH, Dennison C, Vuilleumier S. Methanobactin and the link between copper and bacterial methane oxidation. Microbiol Mol Biol Rev. 2016;80:387–409.CAS 
Article 

Google Scholar 
7.Kenney GE, Rosenzweig AC. Genome mining for methanobactins. BMC Biol. 2013;11:17.CAS 
Article 

Google Scholar 
8.Yu Z, Zheng Y, Huang J, Chistoserdova L. Systems biology meets enzymology: recent insights into communal metabolism of methane and the role of lanthanides. Curr Issues Mol Biol. 2019;33:183–96.Article 

Google Scholar 
9.Gwak J-H, Jung M-Y, Hong HY, Kim J-G, Quan Z-X, Reinfelder JR, et al. Archaeal nitrification is constrained by copper complexation with organic matter in municipal wastewater treatment plants. ISME J. 2020;14:335–46.CAS 
Article 

Google Scholar 
10.Chang J, Kim DD, Semrau JD, Lee J, Heo H, Gu W, et al. Enhancement of nitrous oxide emissions in soil microbial consortia via copper competition between proteobacterial methanotrophs and denitrifiers. Appl Environ Microbiol. 2020;87:e02301–20.
Google Scholar  More

Indigenous territories, long a bulwark against deforestation in the Amazon, are under increasing threat in Brazil, according to an analysis of 36 years’ worth of satellite imagery. The data show that illicit mining operations on Indigenous lands and in other areas formally protected by law have hit a record high in the past few years, under the administration of President Jair Bolsonaro, underscoring fears that his policies and rhetoric are undermining both human rights and environmental protection across the world’s largest rainforest. These operations strip the land of vegetation and pollute waterways with mercury.
When will the Amazon hit a tipping point?
The analysis, released in late August, comes as scientists and environmentalists warn of a deteriorating situation in Brazil; Indigenous groups have frequently found themselves in violent clashes with miners since Bolsonaro took office in 2019 — and they are demanding more protection for their land. Although Indigenous territories are legally protected, Bolsonaro has openly called for mining and other development in them.“This is definitely the worst it’s been for Indigenous peoples since the constitution was signed in 1988,” says Glenn Shepard, an anthropologist with the Emílio Goeldi Museum in Belém. Before this, Brazil was ruled by a military dictatorship.Researchers at MapBiomas, a consortium of academic, business and non-governmental organizations that has been conducting geospatial studies across Brazil, developed algorithms that they used in conjunction with Google Earth Engine to conduct the analysis. After training the algorithms on images of mining operations — desolate landscapes where forests have been converted into a collection of sand dunes pockmarked by mining ponds — the team ran its analysis on a freely available archive of imagery captured by the US Landsat programme, and then analysed trends on Indigenous lands and other formally protected areas where mining is not allowed.Over the past decade, illegal mining incursions — mostly small-scale gold extraction operations — have increased fivefold on Indigenous lands and threefold in other protected areas of Brazil such as parks, the data show (see ‘Mining incursions’). The findings agree broadly with reports from Brazil’s National Institute for Space Research (INPE) in São José dos Campos, which monitors the country’s forests and has been issuing alerts about mining incursions for several years. “We kind of knew that this was happening, but to see numbers like this is scary even for us,” says Cesar Diniz, a geologist with the geospatial-analysis company Solved in Belém, Brazil, who led the analysis for MapBiomas.Clashes on multiple frontsAside from being home to their people, Indigenous territories play a part in protecting the Amazon’s biodiversity and the enormous pool of carbon that is locked away in its trees and soils. Numerous studies have found that Indigenous lands, as well as other conservation areas, are effective buffers against tropical deforestation in the Amazon1,2, which is responsible for around 8% of global carbon emissions.Earlier this month, the International Union for Conservation of Nature (IUCN) approved a motion, put forward by Indigenous groups, calling on governments to protect 80% of the Amazon basin by 2025. Indigenous representatives say they plan to fight for implementation across the Amazon, but the proposal faces a particularly tough sell in Brazil under Bolsonaro, whose pro-business conservative government has scaled back enforcement of existing environmental laws and halted efforts to demarcate new Indigenous territories.

Sources: MapBiomas/Amazon Geo-Referenced Socio-Environmental Information Network/Terrabrasilis

Indigenous groups have also taken their case to the International Criminal Court in The Hague, the Netherlands. On 9 August, the Articulation of Indigenous Peoples of Brazil (APIB), which represents Indigenous groups across the country, filed a complaint with the court accusing the Bolsonaro administration of violating human rights and, they claim, paving a path for genocide by undermining Indigenous rights, reducing environmental protections and inciting incursions and violence through calls for mining and land development. APIB also made it clear that it’s not just Indigenous rights at stake, drawing a direct link between the protection of their territories and of the globe.

Members of the Munduruku people sit in front of equipment from an illegal mining operation on their land.Credit: Meridith Kohut/The New York Times/eyevine

“Defending the traditional territories of Amazonian communities is the best way to save the forest,” says Luiz Eloy Terena, an anthropologist and lawyer from the village of Ipegue who coordinates legal affairs for APIB. “What is needed is a state commitment on the demarcation and protection of Indigenous lands, which are the last barrier against deforestation and forest degradation.”During an address to the United Nations General Assembly on 21 September, Bolsonaro said he was committed to protecting the Amazon and emphasized that 600,000 Indigenous people live “in freedom” on reserves totalling 1.1 million square kilometres of land, equivalent to 14% of Brazil’s territory. In the past, Bolsonaro has publicly said that Indigenous peoples have too much land given their sparse population, and at times called for their “integration”. The Bolsonaro administration did not respond to Nature’s requests for comment regarding illegal mining in the Amazon, its Indigenous and environmental policies or the accusations filed with the International Criminal Court.Existential threatBrazil earned recognition as a leader in sustainable development during the 2000s. Former president Luiz Inácio ‘Lula’ da Silva and his Workers’ Party put in place policies that helped to curb deforestation in the Amazon by more than 80% between 2004 and 2012.

Source: Brazilian National Institute for Space Research

But the party was dogged by corruption charges that would later land Lula in jail, and its environmental agenda ultimately faltered. In 2012, the increasingly conservative Brazilian Congress weakened a once-vaunted forest-protection law. With each successive government, funding for the country’s main environmental enforcement agency, the Institute of Environment and Renewable Natural Resources (IBAMA), has decreased: IBAMA had 1,500 enforcement agents in 2012, compared with just 600 today, says Suely Araújo, a political scientist in Brasília who spent nearly three decades working in the Brazilian Congress and led IBAMA from 2016 to 2018.The rate of deforestation in the Amazon, which includes land converted for mining, agriculture and other development, began rising anew after 2012 and shot up by 44% during Bolsonaro’s first two years in office, according to INPE (see ‘Razing the rainforest’). Many expect yet another increase when the numbers for 2021 are released later this year.But the biggest threats are yet to come, says Araújo. The current government is now pushing legislation in Congress — as well as arguments in a case that is pending before Brazil’s Supreme Court — that would make it harder to establish new Indigenous lands and could even allow the government to repossess existing lands. Other legislation that has been advanced by Bolsonaro’s supporters in Congress would open up Indigenous lands to industrial development, grant amnesty to people who have illegally invaded public lands and gut regulations governing major infrastructure projects such as mines, roads and dams.
The scientists restoring a gold-mining disaster zone in the Peruvian Amazon
“It’s painful,” says Araújo, who decided to forgo retirement and join Brazil’s Climate Observatory, a coalition of activist and academic groups fighting to preserve the country’s social and environmental protections. “This has become my mission.”For Indigenous tribes, the growing damage to their lands and the rainforest pose an existential threat. More than 6,000 Indigenous people descended on Brasília, the country’s capital, in August and September in protest against Bolsonaro’s policies on land demarcation and the environment. They also travelled to Marseille, France, for the IUCN’s World Conservation Congress earlier this month to promote their motion to protect the Amazon basin.“We will not give up,” says José Gregorio Diaz Mirabal, a member of the Wakueni Kurripaco people of Venezuela and the elected leader of the Congress of Indigenous Organizations of the Amazon Basin. “Science supports us, and the world is waking up.”

doi: https://doi.org/10.1038/d41586-021-02644-x

References1.Blackman, A., Corral, L., Lima, E. S. & Asner, G. P. Proc. Natl Acad. Sci. USA 114, 4123–4128 (2017).PubMed 
Article 

Google Scholar 
2.Walker, W. S. et al. Proc. Natl Acad. Sci. USA 117, 3015–3025 (2020).PubMed 
Article 

Google Scholar 
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OUTLOOK
29 September 2021

Why stem cells might save the northern white rhino

Biologist Jeanne Loring explains how her work could bring endangered animal species back from the brink.

Julianna Photopoulos

Julianna Photopoulos

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Stem-cell researcher Jeanne Loring in her laboratory at Scripps Research.Credit: Nelvin C. Cepeda/SDU-T/Zuma/eyevine

Up to one million plant and animal species face extinction, many within decades, because of human activities. One of these is the northern white rhinoceros (Ceratotherium simum cottoni). Only two individuals remain, both of them female, making the subspecies functionally extinct. Jeanne Loring, a stem-cell biologist and founding director of the Center for Regenerative Medicine at Scripps Research in La Jolla, California, spoke to Nature about how collecting and reprogramming stem cells could save this species and others from extinction.What does stem-cell research have to do with saving endangered animals?Induced pluripotent stem (iPS) cells, which closely resemble embryonic stem cells, can develop into any tissue in the body, including sperm and eggs. The hope is to generate these reproductive cells from the reprogrammed stem cells of endangered animals, and use them in assisted captive-breeding programmes to rescue the species.How did you get involved in this work?My laboratory set out to make iPS cells from endangered animals in 2008, after we visited the San Diego Zoo Safari Park in California. The previous year, a team led by Shinya Yamanaka, who won a Nobel prize for the work, had become the first to make human iPS cells from skin cells called fibroblasts1, and we had immediately started making them too, to treat neurological diseases. The San Diego Zoo’s Institute for Conservation Research had been collecting and freezing fibroblasts from animals since the 1970s. The institute’s director of conservation genetics, Oliver Ryder, was thinking of using stem cells to try to treat musculoskeletal disorders, but nobody had created iPS cells from endangered species before.
Part of Nature Outlook: Stem cells
In 2011, my postdoctoral fellow Inbar Friedrich Ben-Nun was the first to reprogramme stem cells in two animals from endangered species: the northern white rhino and the drill monkey (Mandrillus leucophaeus)2. We’re now focused on saving the northern white rhino — Ryder’s favourite animal — but the techniques we are working on are going to become a standard way of rescuing species from extinction.When did this become a serious venture?Our endangered-species project mostly remained a hobby until 2015, when scientists and conservationists from around the world met in Vienna to explore how cell technologies might aid conservation. We seriously discussed the idea of using stem cells to rescue endangered species, and later published a rescue plan for the northern white rhino3. To begin with, embryos will be created from sperm and egg cells that were collected and stored. They’ll then be implanted into a surrogate mother, a southern white rhino (Ceratotherium simum simum). But we want to be able to create more sperm and eggs from iPS cells and implant them, too — and that’s where our team comes in.After the Vienna meeting, the San Diego Zoo invested in this idea. Staff there built a stem-cell lab and the Rhino Rescue Center, where they brought in six southern white rhinos from Africa, specifically to serve as surrogate mothers for embryos made from northern white rhinos’ cells. The animals should be compatible because southern white and northern white rhinos are closely related, and so have similar reproductive physiologies. A team of reproductive biologists led by Barbara Durrant is now working to perfect the techniques to fertilize eggs in vitro and transfer viable embryos into the southern white rhinos.What progress have you made in creating northern white rhinoceros iPS cells?When we first set out to make the cells from endangered animals, we assumed that human versions of the reprogramming genes would not work in a rhino. So we tried reprogramming the rhino’s fibroblasts with horse genes — the horse is one of the closest relatives of the rhino — but this failed. Surprisingly, the corresponding human genes did work, and we were able to generate pluripotent cells. However, we had used viral vectors to reprogramme the cells, and this has been shown to lead to tumours in mice, so it could not be used for reproduction purposes.After three years of tweaking the technique, we were able to perform the reprogramming without any genetic modification. It’s all trial and error — you just have to keep testing different combinations of variables. Earlier this year, we celebrated a milestone in our efforts to rescue the rhino: Marisa Korody’s lab at the San Diego Zoo was able to reprogramme frozen cells from nine northern white rhinos and two southern white females to become iPS cells4.

Najin (right) and her daughter Fatu are the world’s only remaining northern white rhinos.Credit: Tony Karumba/AFP via Getty

How do you hope to create gametes from iPS cells?The major effort now is to make eggs that can be fertilized with sperm collected from adult males. We’re following in the footsteps of other researchers who have had success, mainly with mice so far. For example, in 2016, Katsuhiko Hayashi and his team at Kyushu University in Fukuoka, Japan, artificially engineered egg cells from reprogrammed mouse skin cells, entirely in a dish, and these were used to birth pups that were healthy and fertile5.That technique required ovarian tissue to be co-cultured with the developing eggs to get them to mature, and it’s impossible to get that kind of tissue from rhinos without putting them at risk. But in July, the same team showed that it could make both egg cells and ovarian tissue from iPS cells, which was a huge improvement6.We are now trying to find an efficient way to make the precursors of gametes, known as primordial germ cells, from the iPS cells of northern white rhinos. We know it’s possible — we’ve seen it happen spontaneously in cultures of these iPS cells — but we need to learn how to generate more of them. And then we have to turn those germ cells into eggs and sperm — or at least, something like sperm. Typically, the process of in vitro fertilization (IVF) involves knocking the tail off a sperm cell and injecting the small head directly into the egg, so we might not need to make sperm with tails. The IVF process itself will need to be adapted, however, to the southern white rhino surrogates — we don’t know for sure that it will work as it does in humans, because it’s never been done before.What advantage is there to using stem-cell technology over other approaches, such as cloning?The San Diego Zoo has frozen fibroblasts from 12 northern white rhinos. We didn’t want to clone those animals, because we would still have only the same 12 individuals. But if we make gametes from them instead — sperm from males, eggs from females and, in theory, sperm from females — then we could make various combinations through IVF to get a new, genetically diverse pool of animals that will help the species to survive. We have found that there is sufficient diversity in combining that group of 12 to exceed the diversity of the current population of southern white rhinos.
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Another group, at the Leibniz Institute for Zoo and Wildlife Research in Berlin, is instead harvesting eggs from the two living animals in the hope that they can fertilize them and get new animals that way. I’m perfectly happy if that works, but the challenge is getting enough diversity in the population if you have eggs from only one or two animals.Have you encountered opposition to your iPS-cell-mediated approach?If I were doing this with humans there’d be a lot of debate, but with animals there is less. One criticism is that resources for conservation should be invested differently, for example in restoring natural habitats and educating people. One argument we hear is that there’s no purpose in rescuing a species that will be confined to zoos because of poaching. I don’t know how to stop people from hunting rhinos for their horns, but I will do what I can to try to save an animal that humans have forced into extinction.Are you confident that your work will help to save the northern white rhino?It saddens me that as we’ve made progress in the lab, these animals have been dying out. When we started this project there were 8 of them alive, and now there are only 2: Najin, aged 32, and her daughter Fatu, aged 21, who live in a protected park in Kenya. It’s possible that these last two survivors will be gone by the time we succeed. I hope that’s not the case, but we’re working with cells that have been harvested and frozen, so we can try to bring the species back to life if necessary.I can’t predict how long it will take to get there — things have happened much more slowly than I’d like. But I do hope that our efforts will pay off over the next 10 to 20 years. I want to see a new northern white rhino in my lifetime — before I become ‘extinct’!

Nature 597, S18-S19 (2021)
doi: https://doi.org/10.1038/d41586-021-02626-zThis interview has been edited for length and clarity.This article is part of Nature Outlook: Stem cells, an editorially independent supplement produced with the financial support of third parties. About this content.

References1.Takahashi, K. et al. Cell 131, 861–872 (2007).PubMed 
Article 

Google Scholar 
2.Ben-Nun, I. F. et al. Nature Methods 8, 829–831 (2011).PubMed 
Article 

Google Scholar 
3.Saragusty, J. et al. Zoo Biol. 35, 280–292 (2016).PubMed 
Article 

Google Scholar 
4.Korody, M. L. et al. Stem Cells Dev. 30, 177–189 (2021).PubMed 
Article 

Google Scholar 
5.Hikabe, O. et al. Nature 539, 299–303 (2016).PubMed 
Article 

Google Scholar 
6.Yoshino, T. et al. Science 373, eabe0237 (2021).PubMed 
Article 

Google Scholar 
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1.Turner, W. R. et al. Global conservation of biodiversity and ecosystem services. Bioscience 57, 868–873. https://doi.org/10.1641/B571009 (2007).Article 

Google Scholar 
2.O’Connor, B., Bojinski, S., Roosli, C. & Schaepman, M. E. Monitoring global changes in biodiversity and climate essential as ecological crisis intensifies. Ecol. Inform. https://doi.org/10.1016/j.ecoinf.2019.101033 (2020).Article 

Google Scholar 
3.Driscoll, D. A. et al. A biodiversity-crisis hierarchy to evaluate and refine conservation indicators. Nat. Ecol. Evolut. 2, 775–781. https://doi.org/10.1038/s41559-018-0504-8 (2018).Article 

Google Scholar 
4.Mouillot, D. et al. Rare species support vulnerable functions in high-diversity ecosystems. PLoS. Biol. 11, 11. https://doi.org/10.1371/journal.pbio.1001569 (2013).CAS 
Article 

Google Scholar 
5.Hughes, T. P., Graham, N. A. J., Jackson, J. B. C., Mumby, P. J. & Steneck, R. S. Rising to the challenge of sustaining coral reef resilience. Trends Ecol. Evol. 25, 633–642. https://doi.org/10.1016/j.tree.2010.07.011 (2010).Article 
PubMed 

Google Scholar 
6.Hughes, T. P. et al. Global warming transforms coral reef assemblages. Nature 556, 492 (2018).ADS 
CAS 
Article 
PubMed 

Google Scholar 
7.Säterberg, T., Sellman, S. & Ebenman, B. High frequency of functional extinctions in ecological networks. Nature 499, 468–470 (2013).ADS 
Article 
PubMed 

Google Scholar 
8.Valiente-Banuet, A. et al. Beyond species loss: The extinction of ecological interactions in a changing world. Funct. Ecol. 29, 299–307 (2015).Article 

Google Scholar 
9.Fontoura, L. et al. Climate-driven shift in coral morphological structure predicts decline of juvenile reef fishes. Glob. Change Biol. 26, 557–567. https://doi.org/10.1111/gcb.14911 (2020).ADS 
Article 

Google Scholar 
10.Chivers, D. P., McCormick, M. I., Allan, B. J. & Ferrari, M. C. O. Risk assessment and predator learning in a changing world: Understanding the impacts of coral reef degradation. Sci. Rep. 6, 32542 (2016).ADS 
CAS 
Article 
PubMed 

Google Scholar 
11.Downie, A. T. et al. Exposure to degraded coral habitat depresses oxygen uptake rate during exercise of a juvenile reef fish. Coral Reefs https://doi.org/10.1007/s00338-021-02113-x (2021).Article 

Google Scholar 
12.Ferrari, M. C. O., McCormick, M. I., Allan, B. J. & Chivers, D. P. Not equal in the face of habitat change: Closely related fishes differ in their ability to use predation-related information in degraded coral. Proc. R. Soc. B 284, 20162758 (2017).Article 
PubMed 

Google Scholar 
13.McCormick, M. I., Barry, R. P. & Allan, B. J. M. Algae associated with coral degradation affects risk assessment in coral reef fishes. Sci. Rep. 7, 12. https://doi.org/10.1038/s41598-017-17197-1 (2017).CAS 
Article 

Google Scholar 
14.Brown, G. E. & Chivers, D. P. in Fish cognition and behaviour (eds C. Brown, K. Laland, & J. Krause) 49–69 (Blackwell Scientific Publisher, 2006).15.Meuthen, D., Baldauf, S. A., Bakker, T. C. M. & Thunken, T. Neglected patterns of variation in phenotypic plasticity: Age- and sex-specific antipredator plasticity in a cichlid fish. Am. Nat. 191, 475–490. https://doi.org/10.1086/696264 (2018).Article 

Google Scholar 
16.Lonnstedt, O. M., McCormick, M. I., Meekan, M. G., Ferrari, M. C. O. & Chivers, D. P. Learn and live: Predator experience and feeding history determines prey behaviour and survival. Proc. R. Soc. B-Biol. Sci. 279, 2091–2098. https://doi.org/10.1098/rspb.2011.2516 (2012).Article 

Google Scholar 
17.Ferrari, M. C. O. et al. School is out on noisy reefs: The effect of boat noise on predator learning and survival of juvenile coral reef fishes. Proc. R. Soc. B-Biol. Sci. 285, 8. https://doi.org/10.1098/rspb.2018.0033 (2018).Article 

Google Scholar 
18.Chivers, D. P., McCormick, M. I., Mitchell, M. D., Ramasamy, R. A. & Ferrari, M. C. O. Background level of risk determines how prey categorize predators and non-predators. Proc. R. Soc. B 281, 20140355 (2014).Article 
PubMed 

Google Scholar 
19.Crane, A. L. & Ferrari, M. C. O. in Social learning theory: Phylogenetic considerations across animal, plant, and microbial taxa (ed K. B. Clark) 53–82 (Nova Science Publishers, 2013).20.Ferrari, M. C. O., Wisenden, B. D. & Chivers, D. P. Chemical ecology of predator–prey interactions in aquatic ecosystems: A review and prospectus. Can. J. Zool. 88, 698–724 (2010).Article 

Google Scholar 
21.Mirza, R. S. & Chivers, D. P. Are chemical alarm cues conserved within salmonid fishes?. J. Chem. Ecol. 27, 1641–1655 (2001).CAS 
Article 

Google Scholar 
22.Brown, G. E., Adrian, J. C., Naderi, N. T., Harvey, M. C. & Kelly, J. M. Nitrogen oxides elicit antipredator responses in juvenile channel catfish, but not in convict cichlids or rainbow trout: Conservation of the ostariophysan alarm pheromone. J. Chem. Ecol. 29, 1781–1796 (2003).CAS 
Article 

Google Scholar 
23.Pollock, M. S., Chivers, D. P., Mirza, R. S. & Wisenden, B. D. Fathead minnows, Pimephales promelas, learn to recognize chemical alarm cues of introduced brook stickleback, Culaea inconstans. Environ. Biol. Fishes 66, 313–319 (2003).Article 

Google Scholar 
24.Chivers, D. P., Brown, G. E. & Smith, R. J. F. Acquired recognition of chemical stimuli from pike, Esox lucius, by brook sticklebacks, Culaea inconstans (Osteichthyes, Gasterosteidae). Ethology 99, 234–242 (1995).Article 

Google Scholar 
25.Mitchell, M. D., Cowman, P. F. & McCormick, M. I. Chemical alarm cues are conserved within the coral reef fish family Pomacentridae. Plos One 7, e47428 (2012).ADS 
CAS 
Article 
PubMed 

Google Scholar 
26.Ferrari, M. C. O. et al. Intrageneric variation in antipredator responses of coral reef fishes affected by ocean acidification: implications for climate change projections on marine communities. Glob. Change Biol. 17, 2980–2986 (2011).ADS 
Article 

Google Scholar 
27.Chivers, D. et al. Coral degradation alters predator odour signatures and influences prey learning and survival. Proc. R. Soc. B 286, 20190562 (2019).CAS 
Article 
PubMed 

Google Scholar 
28.Ferrari, M. C. O., McCormick, M. I., Meekan, M. G. & Chivers, D. P. Background level of risk and the survival of predator-naive prey: Can neophobia compensate for predator naivety in juvenile coral reef fishes?. Proc. R. Soc. Lond. B Biol. Sci. 282, 20142197 (2015).
Google Scholar 
29.Stewart, B. D. & Beukers, J. S. Baited technique improves censuses of cryptic fish in complex habitats. Mar. Ecol. Prog. Ser. 197, 259–272 (2000).ADS 
Article 

Google Scholar 
30.Hoey, A. S. & McCormick, M. I. in Proceedings of the 10th international coral reef symposium Vol. 1. 420–424 (2006).31.McCormick, M. I., Chivers, D. P., Allan, B. J. & Ferrari, M. C. O. Habitat degradation disrupts neophobia in juvenile coral reef fish. Glob. Change Biol. 23, 719–727 (2017).ADS 
Article 

Google Scholar 
32.McCormick, M. I., Moore, J. A. Y. & Munday, P. L. Influence of habitat degradation on fish replenishment. Coral Reefs 29, 537–546. https://doi.org/10.1007/s00338-010-0620-7 (2010).ADS 
Article 

Google Scholar 
33.McCormick, M. I. Behaviourally mediated phenotypic selection in a disturbed coral reef environment. Plos One https://doi.org/10.1371/journal.pone.0007096 (2009).Article 
PubMed Central 
PubMed 

Google Scholar 
34.White, J. R., Meekan, M. G. & McCormick, M. I. Individual consistency in the behaviors of newly-settled reef fish. PeerJ 3, e961 (2015).Article 
PubMed 

Google Scholar 
35.McCormick, M. I. & Weaver, C. J. It pays to be pushy: Intracohort interference competition between two reef fishes. Plos One 7, e42590 (2012).ADS 
CAS 
Article 
PubMed 

Google Scholar 
36.Wolf, N. G. Odd fish abandon mixed-species groups when threatened. Behav. Ecol. Sociobiol. 17, 47–52 (1985).Article 

Google Scholar 
37.Usio, N., Konishi, M. & Nakano, S. Species displacement between an introduced and a ‘vulnerable’ crayfish: The role of aggressive interactions and shelter competition. Biol. Invasions 3, 179–185 (2001).Article 

Google Scholar 
38.Dargent, F., Torres-Dowdall, J., Scott, M. E., Ramnarine, I. & Fussmann, G. F. Can mixed-species groups reduce individual parasite load? A field test with two closely related poeciliid fishes (Poecilia reticulata and Poecilia picta). PloS One 8, e56789 (2013).ADS 
CAS 
Article 
PubMed 

Google Scholar 
39.Uetz, G. W. & Hieber, C. S. Group size and predation risk in colonial web-building spiders: Analysis of attack abatement mechanisms. Behav. Ecol. 5, 326–333 (1994).Article 

Google Scholar 
40.McCormick, M. I., Barry, R. P. & Allan, B. J. Algae associated with coral degradation affects risk assessment in coral reef fishes. Sci. Rep. 7, 16937 (2017).ADS 
Article 
PubMed 

Google Scholar 
41.Lecchini, D., Planes, S. & Galzin, R. Experimental assessment of sensory modalities of coral-reef fish larvae in the recognition of their settlement habitat. Behav. Ecol. Sociobiol. 58, 18–26. https://doi.org/10.1007/s00265-004-0905-3 (2005).Article 

Google Scholar 
42.Lecchini, D., Planes, S. & Galzin, R. The influence of habitat characteristics and conspecifics on attraction and survival of coral reef fish juveniles. J. Exp. Mar. Biol. Ecol. 341, 85–90. https://doi.org/10.1016/j.jembe.2006.10.006 (2007).Article 

Google Scholar 
43.Lecchini, D., Waqalevu, V. P., Parmentier, E., Radford, C. A. & Banaigs, B. Fish larvae prefer coral over algal water cues: Implications of coral reef degradation. Mar. Ecol. Prog. Ser. 475, 303–307. https://doi.org/10.3354/meps10094 (2013).ADS 
Article 

Google Scholar 
44.O’Connor, J. J. et al. Sediment pollution impacts sensory ability and performance of settling coral-reef fish. Oecologia 180, 11–21. https://doi.org/10.1007/s00442-015-3367-6 (2016).ADS 
Article 

Google Scholar 
45.Chivers, D. P. & Smith, R. J. F. Chemical alarm signalling in aquatic predator–prey systems: A review and prospectus. Ecoscience 5, 338–352 (1998).Article 

Google Scholar 
46.Wisenden, B. D. Olfactory assessment of predation risk in the aquatic environment. Philos. Trans. R. Soc. Lond. Ser. B Biol. Sci. 355, 1205–1208 (2000).CAS 
Article 

Google Scholar 
47.Brown, G. E., Adrian, J. C., Smyth, E., Leet, H. & Brennan, S. Ostariophysan alarm pheromones: Laboratory and field tests of the functional significance of nitrogen oxides. J. Chem. Ecol. 26, 139–154 (2000).CAS 
Article 

Google Scholar 
48.Bertucci, F. et al. Decreased retention of olfactory predator recognition in juvenile surgeon fish exposed to pesticide. Chemosphere 208, 469–475 (2018).ADS 
CAS 
Article 
PubMed 

Google Scholar 
49.Mitchell, M. D., McCormick, M. I., Ferrari, M. C. O. & Chivers, D. P. Coral reef fishes rapidly learn to identify multiple unknown predators upon recruitment to the reefs. Plos One 6, e15764 (2011).ADS 
CAS 
Article 
PubMed 

Google Scholar 
50.Palacios, M., Malerba, M. & McCormick, M. Multiple predator effects on juvenile prey survival. Oecologia 188, 417–427 (2018).ADS 
CAS 
Article 

Google Scholar 
51.Auster, P. J., Cortés, J., Alvarado, J. J. & Beita-Jiménez, A. Coordinated hunting behaviors of mixed-species groups of piscivores and associated species at Isla del Coco National Park (Eastern Tropical Pacific). Neotrop. Ichthyol. 17, e180165 (2019).Article 

Google Scholar 
52.Pandolfi, J. M. et al. Global trajectories of the long-term decline of coral reef ecosystems. Science 301, 955–958 (2003).ADS 
CAS 
Article 

Google Scholar 
53.Cheng, L. et al. 2018 Continues record global ocean warming. Adv. Atmos. Sci. 36, 249–252. https://doi.org/10.1007/s00376-019-8276-x (2019).Article 

Google Scholar 
54.Lawton, J. H. & Brown, V. K. Redundancy in ecosystems Vol. 99 (Springer, 1993).
Google Scholar  More

1.Stein, R. & Macdonald, R. W. Organic carbon budget: Arctic Ocean vs. global ocean. In The Organic Carbon Cycle in the Arctic Ocean (eds Stein, R. & Macdonald, R. W.) (Springer, 2004).Chapter 

Google Scholar 
2.Barber, D. G. & Massom, R. A. The role of sea ice in Arctic and Antarctic polynyas. Oceanogr. Ser. 74, 1–54. https://doi.org/10.1016/S0422-9894(06)74001-6 (2007).Article 

Google Scholar 
3.Sheremetevskiy, A. M. Role of meiobenthos of the South Sakhalin shelf, Eastern Kamchatka, and Novosibirsk shallow water area. Issledovaniya Fauny Morei 35, 43 (1987).
Google Scholar 
4.Golikov, A. N. Ecosystems of the New Siberian shoals and fauna of the Laptev Sea and adjacent waters of the Arctic Ocean (in Russian). Explor. Fauna Seas 37, 4 (1990).
Google Scholar 
5.Golikov, A. N. Fauna of the East Siberian Sea. Part III. Explor. Fauna Seas 49, 57 (1994).
Google Scholar 
6.Sirenko, B. I. & Denisenko, S. G. Fauna of the East Siberian Sea, distribution patterns and structure of bottom communities. Explor. Fauna Seas 66, 74 (2010).
Google Scholar 
7.Sirenko, B. I. List of species of free-living invertebrates of Eurasian Arctic seas and adjacent deep waters. Explor. Fauna Seas 51(59), 1–76 (2001).
Google Scholar 
8.Schmidt-Rhaesa, A. Handbook of Zoology: Gastrotricha, Cycloneuralia, Gnathifera Vol. 2, 608 (De Gruyter, 2020).
Google Scholar 
9.Udalov, A. et al. Integrity of benthic assemblages along the arctic estuarine-coastal system. Ecol. Indic. 121, 107115. https://doi.org/10.1016/j.ecolind.2020.107115 (2021).Article 

Google Scholar 
10.Portnova, D., Fedyaeva, M., Udalov, A. & Tchesunov, A. Community structure of nematodes in the Laptev Sea shelf with notes on the lives of ice nematodes. Reg. Stud. Mar. Sci. 31, 100757. https://doi.org/10.1016/j.rsma.2019.100757 (2019).Article 

Google Scholar 
11.Gallucci, F., Moens, T. & Fonseca, G. Small-scale spatial patterns of meiobenthos in the Arctic deep sea. Mar. Biodivers. 39(1), 9–25. https://doi.org/10.1007/s12526-009-0003-x (2009).Article 

Google Scholar 
12.Lei, Y., Stumm, K., Volkenborn, N., Wickham, S. A. & Berninger, U. G. Impact of Arenicola marina (Polychaeta) on the microbial assemblages and meiobenthos in a marine intertidal flat. Mar. Biol. 157(6), 1271–1282. https://doi.org/10.1007/s00227-010-1407-7 (2010).Article 

Google Scholar 
13.Flint, M. V., Poyarkov, S. G. & Rymsky-Korsakov, N. A. Ecosystems of the Siberian Arctic Seas-2017 (Cruise 69 of the R/V Akademik Mstislav Keldysh). Oceanology 58(2), 315–318. https://doi.org/10.1134/S0001437018020042 (2018).ADS 
Article 

Google Scholar 
14.Garlitska, L. A. & Azovsky, A. I. Benthic harpacticoid copepods of the Yenisei Gulf and the adjacent shallow waters of the Kara Sea. J. Nat. Hist. 50, 2941–2959. https://doi.org/10.1080/00222933.2016.1219410 (2016).Article 

Google Scholar 
15.Portnova, D., Garlitska, L., Udalov, A. & Kondar, D. Meiobenthos and nematode community in the Yenisei Bay and adjacent parts of the Kara Sea shelf. Oceanology 57(1), 1–15. https://doi.org/10.1134/S0001437017010155 (2017).Article 

Google Scholar 
16.Carmack, E. et al. Toward quantifying the increasing role of oceanic heat in sea ice loss in the new Arctic. Bull. Am. Meteorol. Soc. 96(12), 2079–2105. https://doi.org/10.1175/BAMS-D-13-00177.1 (2005).ADS 
Article 

Google Scholar 
17.Peterson, B. J. et al. Increasing river discharge to the Arctic Ocean. Science 298(5601), 2171–2173. https://doi.org/10.1126/science.1077445 (2002).ADS 
CAS 
Article 
PubMed 

Google Scholar 
18.Polukhin, A. The role of river runoff in the Kara Sea surface layer acidification and carbonate system changes. ERL 14(10), 105007. https://doi.org/10.1088/1748-9326/ab421e (2019).ADS 
CAS 
Article 

Google Scholar 
19.Lisitzin, A. P. Marginal filter of the oceans. Oceanology 34(5), 735–743 (1994).CAS 

Google Scholar 
20.Moens, T., Braeckman, U., Derycke, S., Fonseca, G., Gallucci, F., Gingold, R., Guilini, Katja, Ingles, J., Leduc, D., Vanaverbeke, J., Van Colen, C., Vanreusel, A, & Vincx, M. Ecology of free-living marine nematodes. In Volume 2 Nematoda, 109–152. De Gruyter (2013)21.Aller, J. Y. & Aller, R. C. General characteristics of benthic faunas on the Amazon inner continental shelf with comparison to the shelf off the Changjiang River, East China Sea. Cont. Shelf Res. 6(1–2), 291–310. https://doi.org/10.1016/0278-4343(86)90065-8 (1986).ADS 
Article 

Google Scholar 
22.Soetaert, K., Vincx, M., Wittoeck, J. & Tulkens, M. Meiobenthic distribution and nematode community structure in five European estuaries. Hydrobiologia 311(1), 185–206. https://doi.org/10.1007/BF00008580 (1995).Article 

Google Scholar 
23.Tank, S. E. et al. The processing and impact of dissolved riverine nitrogen in the Arctic Ocean. Estuaries Coast 35, 401–415. https://doi.org/10.1007/s12237-011-9417-3 (2012).CAS 
Article 

Google Scholar 
24.Galtsova, V. V., Lukina, T. G. & Vladimirov, M. V. Meiobenthos of Chaunskaya Bay, East Siberian Sea. Issledovaniya Fauny Morei 48(56), 67–97 (1994).
Google Scholar 
25.Coull, B. C. Role of meiofauna in estuarine soft‐bottom habitats. Austral Ecol. 24(4), 327–343 (1999).Article 

Google Scholar 
26.Vincx, M., Meire, P., & Heip, C. The distribution of nematodes communities in the Southern Bight of the North Sea. Cah Biol Mar. 31(1), 107–129 (1990).27.Vanaverbeke, J., Gheskiere, T., Steyaert, M., & Vincx, M. Nematode assemblages from subtidal sandbanks in the Southern Bight of the North Sea: effect of small sedimentological differences. J. Sea Res. 48(3), 197–207. https://doi.org/10.1016/S1385-1101(02)00165-X (2002)ADS 
Article 

Google Scholar 
28.Steyaert, M., et al. The importance of fine-scale, vertical profiles in characterising nematode community structure. Estuar Coast Shelf Sci. 58(2), 353–366 (2003).ADS 
Article 

Google Scholar 
29.Alves, A. S., Adão, H., Patrício, J., Neto, J. M., Costa, M. J., & Marques, J. C. Spatial distribution of subtidal meiobenthos along estuarine gradients in two southern European estuaries (Portugal). J. Mar. Biol. Assoc. U. K. 89(8), 1529–1540 (2009).CAS 
Article 

Google Scholar 
30.Garlitska, L. A., Chertoprud, E. S., Portnova, D. A. & Azovsky, A. I. Benthic harpacticoida of the Kara Sea: Species composition and bathymetrically related distribution. Oceanology 59(4), 541–551. https://doi.org/10.1134/S0001437019040064 (2019).ADS 
CAS 
Article 

Google Scholar 
31.Huang, D. et al. Preliminary study on community structures of meiofauna in the middle and eastern Chukchi Sea. Acta Oceanol. Sin. 40(6), 83–91. https://doi.org/10.1007/s13131-021-1777-3 (2021).ADS 
Article 

Google Scholar 
32.Giere, O. Meiobenthology: The Microscopic Motile Fauna in Aquatic Sediments 2nd edn. (Springer, 2009).
Google Scholar 
33.Semiletov, I. et al. The East Siberian Sea as a transition zone between Pacific-derived waters and Arctic shelf waters. Geophys. Res. Lett. https://doi.org/10.1029/2005GL022490 (2005).Article 

Google Scholar 
34.Miroshnikov, A. Y. et al. Ecological state and mineral-geochemical characteristics of the bottom sediments of the East Siberian Sea. Oceanology 60(4), 595–610. https://doi.org/10.31857/S0030157420040152 (2020).Article 

Google Scholar 
35.Frontalini, F. et al. The response of cultured meiofaunal and benthic foraminiferal communities to lead exposure: Results from mesocosm experiments. Environ. Toxicol. Chem. 37(9), 2439–2447. https://doi.org/10.1002/etc.4207 (2018).CAS 
Article 
PubMed 

Google Scholar 
36.Fonseca, G. & Soltwedel, T. Deep-sea meiobenthic communities underneath the marginal ice zone off Eastern Greenland. Polar Biol. 30, 607–618. https://doi.org/10.1007/s00300-006-0220-8 (2007).Article 

Google Scholar 
37.Portnova, D. & Polukhin, A. Meiobenthos of the eastern shelf of the Kara Sea compared with the meiobenthos of other parts of the sea. Reg. Stud. Mar. Sci. 24, 370–378. https://doi.org/10.1016/j.rsma.2018.10.002 (2018).Article 

Google Scholar 
38.Alexeev, D. K., & Galtsova, V. V. Effect of radioactive pollution on the biodiversity of marine benthic ecosystems of the Russian Arctic shelf. Polar Sci. 6(2), 183–195 (2012).ADS 
Article 

Google Scholar 
39.Grzelak, K. & Sørensen, M. V. Diversity and community structure of kinorhynchs around Svalbard: First insights into spatial patterns and environmental drivers. Zool. Anz. 282, 31–43. https://doi.org/10.1016/j.jcz.2019.05.009 (2019).Article 

Google Scholar 
40.Landers, S. C. et al. Kinorhynch communities from Alabama coastal waters. Mar. Biol. Res. 16(6–7), 494–504. https://doi.org/10.1080/17451000.2020.1789660 (2020).Article 

Google Scholar 
41.Holovachov, O. New and known species of the genus Campylaimus Cobb, 1920 (Nematoda: Araeolaimida: Diplopeltidae) from North European marine habitats. Biodivers. Data J. https://doi.org/10.3897/BDJ.7.e46545 (2007).Article 

Google Scholar 
42.Sharma, J. & Bluhm, B. A. Diversity of larger free-living nematodes from macrobenthos ( > 250 μm) in the Arctic deep-sea Canada Basin. Mar. Biodivers. 41(3), 455–465. https://doi.org/10.1007/s12526-010-0060-1 (2010).Article 

Google Scholar 
43.Kotwicki, L., Grzelak, K. & Bełdowski, J. Benthic communities in chemical munitions dumping site areas within the Baltic deeps with special focus on nematodes. Deep Sea Res. II 128, 123–130. https://doi.org/10.1016/j.dsr2.2015.12.012 (2016).CAS 
Article 

Google Scholar 
44.Netto, S. A., Pagliosa, P. R., Colling, A., Fonseca, A. L. & Brauk, K. M. Benthic estuarine assemblages from the Southern Brazilian marine ecoregion. Braz. Estuaries. https://doi.org/10.1007/978-3-319-77779-5_6 (2018).Article 

Google Scholar 
45.Broman, E., et al. Uncovering diversity and metabolic spectrum of animals in dead zone sediments. Commun. Biol. 3(1), 1–12 (2020).46.Zeppilli, D., et al. Characteristics of meiofauna in extreme marine ecosystems: a review. Mar. Biodiver. 48(1), 35–71 (2018).47.Pérez-García, J. A. et al. Nematode diversity of freshwater and anchialine caves of Western Cuba. PBSW 131(1), 144–155. https://doi.org/10.2988/17-00024 (2018).Article 

Google Scholar 
48.Bezzubova, E. M., Seliverstova, A. M., Zamyatin, I. A. & Romanova, N. D. Heterotrophic bacterioplankton of the Laptev and East Siberian Sea shelf affected by freshwater inflow areas. Oceanology 60, 62–73. https://doi.org/10.1134/S0001437020010026 (2020).ADS 
CAS 
Article 

Google Scholar 
49.Vanreusel, A. et al. Meiobenthos of the central Arctic Ocean with special emphasis on the nematode community structure. Deep Sea Res. I 47, 1855–1879. https://doi.org/10.1016/S0967-063728002900007-8 (2000).Article 

Google Scholar 
50.Tahseen, Q. Nematodes in aquatic environments: Adaptations and survival strategies. Biodivers. J. 3(1), 13–40 (2012).
Google Scholar 
51.Williams, W. J. & Carmack, E. C. The ‘interior’ shelves of the Arctic Ocean: Physical oceanographic setting, climatology and effects of sea-ice retreat on cross-shelf exchange. Prog. Ocean 139, 24–41. https://doi.org/10.1016/j.pocean.2015.07.008 (2015).Article 

Google Scholar 
52.Magritsky, D. V. et al. Long-term changes of river water inflow into the seas of the Russian Arctic sector. Polarforschung 87(2), 177–194. https://doi.org/10.2312/polarforschung.87.2.177 (2018).Article 

Google Scholar 
53.Anderson, L. G. et al. East Siberian Sea, an Arctic region of very high biogeochemical activity. Biogeosciences 4, 6. https://doi.org/10.5194/bg-8-1745-2011 (2011).CAS 
Article 

Google Scholar 
54.Dmitrienko, I. A. et al. Impact of the Arctic Ocean Atlantic water layer on Siberian shelf hydrography. J. Geophys. Res. Oceans. https://doi.org/10.1029/2009JC006020 (2010).Article 

Google Scholar 
55.Stein, R. Arctic Ocean Sediments: Processes, PROXIES, and Paleoenvironment (Elsevier, 2008).
Google Scholar 
56.Petrova, V. I., Batova, G. I., Kursheva, A. V. & Litvinenko, I. V. Geochemistry of organic matter of bottom sediments in the rises of the central Arctic Ocean. Russ. Geol. Geophys. 51(1), 88–97. https://doi.org/10.1016/j.rgg.2009.12.008 (2010).ADS 
Article 

Google Scholar 
57.Millero, F. J. Thermodynamics of the carbon dioxide system in oceans. GCA 59(4), 661–677. https://doi.org/10.12691/wjce-3-6-1 (1995).ADS 
CAS 
Article 

Google Scholar 
58.Pavlova, G. Y. et al. Intercalibration of Bruevich’s method to determine the total alkalinity in seawater. Oceanology 48, 438. https://doi.org/10.1134/S0001437008030168 (2008).ADS 
Article 

Google Scholar 
59.Dickson, A. G. & Goyet, C. Handbook of Methods for the Analysis of the Various Parameters of the Carbon Dioxide System in Sea Water. Version 2 (No. ORNL/CDIAC-74) (1994).60.Dickson, A. G., Afghan, J. D. & Anderson, G. C. Reference materials for oceanic CO2 analysis: A method for the certification of total alkalinity. Mar. Chem. 80, 185–197. https://doi.org/10.1016/S0304-4203(02)00133-0 (2003).CAS 
Article 

Google Scholar 
61.Lewis, E. & Wallace, D. W. R. Program Developed for CO2 System Calculations. ORNL/CDIAC-105 (Carbon Dioxide Information Analysis Center, Oak Ridge National Laboratory, U.S. Department of Energy, 1998).Book 

Google Scholar 
62.Shiklomanov, A. I., Holmes, J. W., McClelland, S. E., Tank, R. & Spencer, G.M. Arctic Great Rivers Observatory. Discharge Dataset, Version 20200801 (2020).63.Niemistö, L. A gravity corer for studies of soft sediments. Merentutkimuslait. Julk./Havsforskningsinst. Skr. 238, 33–38 (1974).
Google Scholar 
64.Eleftheriou, A. Methods for the Study of Marine Benthos (Wiley, 2013).Book 

Google Scholar 
65.Wieser, W. Beziehungen zwischen Mundhöhlengestalt, Ernährungsweise und Vorkommen bei freilebenden, marinen Nematoden. Ark. Zool. 2, 439–484 (1953).
Google Scholar 
66.Hammer, Ø., Harper, D. A. T. & Ryan, P. D. PAST paleontological statistics software package for education and data analysis. Palaeontol. Electron. 4, 1–9 (2001).
Google Scholar 
67.Heip, C. & Herman, P. Indices of diversity and evenness. Oceanis 24(4), 61–88 (2001).
Google Scholar  More