Philippa Kaur

1.
The Global Burden of Disease: 2004 Update (WHO, 2004).
2.
Sheldon, B. C. & Verhulst, S. Ecological immunology: costly parasite defences and trade-offs in evolutionary ecology. Trends Ecol. Evol. 11, 317–321 (1996).
CAS  PubMed  Google Scholar 

3.
Schmid-Hempel, P. Variation in immune defence as a question of evolutionary ecology. Proc. R. Soc. B. 270, 357–366 (2003).
PubMed  Google Scholar 

4.
Schmid-Hempel, P. Evolutionary Parasitology (Oxford Univ. Press, 2013).

5.
Rook, G. A. Regulation of the immune system by biodiversity from the natural environment: an ecosystem service essential to health. Proc. Natl Acad. Sci. USA 110, 18360–18367 (2013).
CAS  PubMed  Google Scholar 

6.
von Hertzen, L., Hanski, I. & Haahtela, T. Natural immunity. Biodiversity loss and inflammatory diseases are two global megatrends that might be related. EMBO Rep. 12, 1089–1093 (2011).
Google Scholar 

7.
Belkaid, Y. & Hand, T. W. Role of the microbiota in immunity and inflammation. Cell 157, 121–141 (2014).
CAS  PubMed  PubMed Central  Google Scholar 

8.
Lambrecht, B. N. & Hammad, H. The immunology of the allergy epidemic and the hygiene hypothesis. Nat. Immunol. 18, 1076–1083 (2017).
CAS  PubMed  Google Scholar 

9.
Rook, G. A., Martinelli, R. & Brunet, L. R. Innate immune responses to mycobacteria and the downregulation of atopic responses. Curr. Opin. Allergy Clin. Immunol. 3, 337–342 (2003).
CAS  PubMed  Google Scholar 

10.
Rosenblum, M. D., Remedios, K. A. & Abbas, A. K. Mechanisms of human autoimmunity. J. Clin. Invest. 125, 2228–2233 (2015).
PubMed  PubMed Central  Google Scholar 

11.
Lafferty, K. D. Biodiversity loss decreases parasite diversity: theory and patterns. Philos. Trans. R. Soc. Lond. B 367, 2814–2827 (2012).
Google Scholar 

12.
Kamiya, T., O’Dwyer, K., Nakagawa, S. & Poulin, R. Host diversity drives parasite diversity: meta-analytical insights into patterns and causal mechanisms. Ecography 37, 689–697 (2014).
Google Scholar 

13.
McDade, T. W., Georgiev, A. V. & Kuzawa, C. W. Trade-offs between acquired and innate immune defenses in humans. Evol. Med. Public Health 2016, 1–16 (2016).
PubMed  PubMed Central  Google Scholar 

14.
Lindstrom, K. M., Foufopoulos, J., Parn, H. & Wikelski, M. Immunological investments reflect parasite abundance in island populations of Darwin’s finches. Proc. R. Soc. B 271, 1513–1519 (2004).
PubMed  Google Scholar 

15.
Mayer, A., Mora, T., Rivoire, O. & Walczak, A. M. Diversity of immune strategies explained by adaptation to pathogen statistics. Proc. Natl Acad. Sci. USA 113, 8630–8635 (2016).
CAS  PubMed  Google Scholar 

16.
Scharsack, J. P., Kalbe, M., Harrod, C. & Rauch, G. Habitat-specific adaptation of immune responses of stickleback (Gasterosteus aculeatus) lake and river ecotypes. Proc. R. Soc. B 274, 1523–1532 (2007).
PubMed  Google Scholar 

17.
Kaczorowski, K. J. et al. Continuous immunotypes describe human immune variation and predict diverse responses. Proc. Natl Acad. Sci. USA 114, E6097–E6106 (2017).
CAS  PubMed  Google Scholar 

18.
Herman, A. et al. The role of gene flow in rapid and repeated evolution of cave-related traits in Mexican tetra, Astyanax mexicanus. Mol. Ecol. 27, 4397–4416 (2018).
CAS  PubMed  PubMed Central  Google Scholar 

19.
Fumey, J. et al. Evidence for late Pleistocene origin of Astyanax mexicanus cavefish. BMC Evol. Biol. 18, 43 (2018).
PubMed  PubMed Central  Google Scholar 

20.
Gibert, J. & Deharveng, L. Subterranean ecosystems: a truncated functional biodiversity. BioScience 52, 473–481 (2002).

21.
Tabin, J. A. et al. Temperature preference of cave and surface populations of Astyanax mexicanus. Dev. Biol. 441, 338–344 (2018).
CAS  PubMed  PubMed Central  Google Scholar 

22.
Abolins, S. et al. The comparative immunology of wild and laboratory mice, Mus musculus domesticus. Nat. Commun. 8, 14811 (2017).
PubMed  PubMed Central  Google Scholar 

23.
Trama, A. M. et al. Lymphocyte phenotypes in wild-caught rats suggest potential mechanisms underlying increased immune sensitivity in post-industrial environments. Cell Mol. Immunol. 9, 163–174 (2012).
CAS  PubMed  PubMed Central  Google Scholar 

24.
Aspiras, A. C., Rohner, N., Martineau, B., Borowsky, R. L. & Tabin, C. J. Melanocortin 4 receptor mutations contribute to the adaptation of cavefish to nutrient-poor conditions. Proc. Natl Acad. Sci. USA 112, 9668–9673 (2015).
CAS  PubMed  Google Scholar 

25.
Xiong, S., Krishnan, J., Peuss, R. & Rohner, N. Early adipogenesis contributes to excess fat accumulation in cave populations of Astyanax mexicanus. Dev. Biol. 441, 297–304 (2018).
CAS  PubMed  Google Scholar 

26.
Wiens, G. D. & Vallejo, R. L. Temporal and pathogen-load dependent changes in rainbow trout (Oncorhynchus mykiss) immune response traits following challenge with biotype 2 Yersinia ruckeri. Fish Shellfish Immunol. 29, 639–647 (2010).
CAS  PubMed  Google Scholar 

27.
Krishnan, J. et al. Comparative transcriptome analysis of wild and lab populations of Astyanax mexicanus uncovers differential effects of environment and morphotype on gene expression. J. Exp. Zool. B https://doi.org/10.1002/jez.b.22933 (2020).

28.
Moller, A. M., Korytar, T., Kollner, B., Schmidt-Posthaus, H. & Segner, H. The teleostean liver as an immunological organ: intrahepatic immune cells (IHICs) in healthy and benzo[a]pyrene challenged rainbow trout (Oncorhynchus mykiss). Dev. Comp. Immunol. 46, 518–529 (2014).
CAS  PubMed  Google Scholar 

29.
Traver, D. et al. Transplantation and in vivo imaging of multilineage engraftment in zebrafish bloodless mutants. Nat. Immunol. 4, 1238–1246 (2003).
CAS  PubMed  Google Scholar 

30.
Stockdale, W. T. et al. Heart regeneration in the Mexican cavefish. Cell Rep. 25, 1997–2007 (2018).
CAS  PubMed  PubMed Central  Google Scholar 

31.
Ramsey, S. et al. Transcriptional noise and cellular heterogeneity in mammalian macrophages. Philos. Trans. R. Soc. Lond. B. 361, 495–506 (2006).
CAS  Google Scholar 

32.
Ogryzko, N. V., Renshaw, S. A. & Wilson, H. L. The IL-1 family in fish: swimming through the muddy waters of inflammasome evolution. Dev. Comp. Immunol. 46, 53–62 (2014).

33.
Wittamer, V., Bertrand, J. Y., Gutschow, P. W. & Traver, D. Characterization of the mononuclear phagocyte system in zebrafish. Blood 117, 7126–7135 (2011).
CAS  PubMed  Google Scholar 

34.
Sunyer, J. O. Evolutionary and functional relationships of B cells from fish and mammals: Insights into their novel roles in phagocytosis and presentation of particulate antigen. Infect. Disord. Drug Targets 12, 200–212 (2012).
CAS  PubMed  PubMed Central  Google Scholar 

35.
Lugo-Villarino, G. et al. Identification of dendritic antigen-presenting cells in the zebrafish. Proc. Natl Acad. Sci. USA 107, 15850–15855 (2010).
CAS  PubMed  Google Scholar 

36.
Haugland, G. T. et al. Phagocytosis and respiratory burst activity in lumpsucker (Cyclopterus lumpus L.) leucocytes analysed by flow cytometry. PLoS ONE 7, e47909 (2012).
CAS  PubMed  PubMed Central  Google Scholar 

37.
Lieschke, G. J. & Trede, N. S. Fish immunology. Curr. Biol. 19, R678–R682 (2009).
CAS  PubMed  Google Scholar 

38.
Balla, K. M. et al. Eosinophils in the zebrafish: prospective isolation, characterization, and eosinophilia induction by helminth determinants. Blood 116, 3944–3954 (2010).
CAS  PubMed  PubMed Central  Google Scholar 

39.
Bolnick, D. I., Shim, K. C., Schmerer, M. & Brock, C. D. Population-specific covariation between immune function and color of nesting male threespine stickleback. PLoS ONE 10, e0126000 (2015).
PubMed  PubMed Central  Google Scholar 

40.
Peuß, R. et al. Label-independent flow cytometry and unsupervised neural network method for de novo clustering of cell populations. Preprint at bioRxiv https://doi.org/10.1101/603035 (2020).

41.
van der Meer, W., Scott, C. S. & de Keijzer, M. H. Automated flagging influences the inconsistency and bias of band cell and atypical lymphocyte morphological differentials. Clin. Chem. Lab. Med. 42, 371–377 (2004).
PubMed  Google Scholar 

42.
Getz, G. S. Thematic review series: the immune system and atherogenesis. Bridging the innate and adaptive immune systems. J. Lipid Res. 46, 619–622 (2005).
CAS  PubMed  Google Scholar 

43.
Wan, F. et al. Characterization of gammadelta T cells from zebrafish provides insights into their important role in adaptive humoral immunity. Front. Immunol. 7, 675 (2016).
PubMed  Google Scholar 

44.
Shilpi, Paul,S. & Lal, G. Role of gamma-delta (gammadelta) T cells in autoimmunity. J. Leukoc. Biol. 97, 259–271 (2015).
PubMed  Google Scholar 

45.
Fan, X. & Rudensky, A. Y. Hallmarks of tissue-resident lymphocytes. Cell 164, 1198–1211 (2016).
CAS  PubMed  PubMed Central  Google Scholar 

46.
Papotto, P. H., Reinhardt, A., Prinz, I. & Silva-Santos, B. Innately versatile: gammadelta17 T cells in inflammatory and autoimmune diseases. J. Autoimmun. 87, 26–37 (2018).
CAS  PubMed  Google Scholar 

47.
Fay, N. S., Larson, E. C. & Jameson, J. M. Chronic Inflammation and gammadelta T. Cells Front. Immunol. 7, 210 (2016).
PubMed  Google Scholar 

48.
Rossi, D. J. et al. Cell intrinsic alterations underlie hematopoietic stem cell aging. Proc. Natl Acad. Sci. USA 102, 9194–9199 (2005).
CAS  PubMed  Google Scholar 

49.
Bolli, N. et al. Expression of the cytoplasmic NPM1 mutant (NPMc+) causes the expansion of hematopoietic cells in zebrafish. Blood 115, 3329–3340 (2010).
CAS  PubMed  PubMed Central  Google Scholar 

50.
Stachura, D. L. et al. Clonal analysis of hematopoietic progenitor cells in the zebrafish. Blood 118, 1274–1282 (2011).
CAS  PubMed  PubMed Central  Google Scholar 

51.
Reavie, L. et al. Regulation of hematopoietic stem cell differentiation by a single ubiquitin ligase-substrate complex. Nat. Immunol. 11, 207–215 (2010).
CAS  PubMed  PubMed Central  Google Scholar 

52.
Cabezas-Wallscheid, N. et al. Identification of regulatory networks in HSCs and their immediate progeny via integrated proteome, transcriptome, and DNA methylome analysis. Cell Stem Cell 15, 507–522 (2014).
CAS  PubMed  Google Scholar 

53.
Cheng, J. et al. Hematopoietic defects in mice lacking the sialomucin CD34. Blood 87, 479–490 (1996).
CAS  PubMed  Google Scholar 

54.
Anjos-Afonso, F. et al. CD34(–) cells at the apex of the human hematopoietic stem cell hierarchy have distinctive cellular and molecular signatures. Cell Stem Cell 13, 161–174 (2013).
CAS  PubMed  Google Scholar 

55.
Amin, R. H. & Schlissel, M. S. Foxo1 directly regulates the transcription of recombination-activating genes during B cell development. Nat. Immunol. 9, 613–622 (2008).
CAS  PubMed  PubMed Central  Google Scholar 

56.
Han, S., Zheng, B., Schatz, D. G., Spanopoulou, E. & Kelsoe, G. Neoteny in lymphocytes: Rag1 and Rag2 expression in germinal center B cells. Science 274, 2094–2097 (1996).
CAS  PubMed  Google Scholar 

57.
Naito, Y. et al. Germinal center marker GL7 probes activation-dependent repression of N-glycolylneuraminic acid, a sialic acid species involved in the negative modulation of B-cell activation. Mol. Cell Biol. 27, 3008–3022 (2007).
CAS  PubMed  PubMed Central  Google Scholar 

58.
Laszlo, G., Hathcock, K. S., Dickler, H. B. & Hodes, R. J. Characterization of a novel cell-surface molecule expressed on subpopulations of activated T and B cells. J. Immunol. 150, 5252–5262 (1993).
CAS  PubMed  Google Scholar 

59.
Fänge, R. & Nilsson, S. The fish spleen: structure and function. Experientia 41, 152–158 (1985).
PubMed  Google Scholar 

60.
Steinel, N. C. & Bolnick, D. I. Melanomacrophage centers as a histological indicator of immune function in fish and other poikilotherms. Front. Immunol. 8, 827 (2017).
PubMed  PubMed Central  Google Scholar 

61.
Cervenak, L., Magyar, A., Boja, R. & Laszlo, G. Differential expression of GL7 activation antigen on bone marrow B cell subpopulations and peripheral B cells. Immunol. Lett. 78, 89–96 (2001).
CAS  PubMed  Google Scholar 

62.
Secombes, C. J., Wang, T. & Bird, S. The interleukins of fish. Dev. Comp. Immunol. 35, 1336–1345 (2011).
CAS  PubMed  Google Scholar 

63.
Weisberg, S. P. et al. Obesity is associated with macrophage accumulation in adipose tissue. J. Clin. Invest. 112, 1796–1808 (2003).
CAS  PubMed  PubMed Central  Google Scholar 

64.
Christ, A. et al. Western diet triggers NLRP3-dependent innate immune reprogramming. Cell 172, 162–175 e114 (2018).
CAS  PubMed  PubMed Central  Google Scholar 

65.
McAlpine, C. S. et al. Sleep modulates haematopoiesis and protects against atherosclerosis. Nature 566, 383–387 (2019).

66.
Heidt, T. et al. Chronic variable stress activates hematopoietic stem cells. Nat. Med. 20, 754–758 (2014).
CAS  PubMed  PubMed Central  Google Scholar 

67.
Mitchell, R. G., Russell, W. H. & Elliott, W. R. Mexican Eyeless Characin Fishes, Genus Astyanax: Environment, Distribution, and Evolution (Texas Tech Press, 1977).

68.
Espinasa, L. et al. A new cave locality for Astyanax cavefish in Sierra de El Abra, Mexico. Subterr. Biol. 26, 39–53 (2018).
Google Scholar 

69.
Embryo Surface Sanitation (Egg Bleaching) Protocol https://zebrafish.org/wiki/protocols/ess (ZIRC, 2019).

70.
Peuß, R., Eggert, H., Armitage, S. A. & Kurtz, J. Downregulation of the evolutionary capacitor Hsp90 is mediated by social cues. Proc. R. Soc. B 282, 20152041 (2015).
PubMed  Google Scholar 

71.
Pfaffl, M. W., Horgan, G. W. & Dempfle, L. Relative expression software tool (REST(C)) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res. 30, 36e (2002).
Google Scholar 

72.
Zhang, Y. A. et al. IgT, a primitive immunoglobulin class specialized in mucosal immunity. Nat. Immunol. 11, 827–835 (2010).
CAS  PubMed  PubMed Central  Google Scholar 

73.
Rowe, R. G., Mandelbaum, J., Zon, L. I. & Daley, G. Q. Engineering hematopoietic stem cells: lessons from development. Cell Stem Cell 18, 707–720 (2016).
CAS  PubMed  PubMed Central  Google Scholar 

74.
Stachura, D. L. et al. The zebrafish granulocyte colony-stimulating factors (Gcsfs): 2 paralogous cytokines and their roles in hematopoietic development and maintenance. Blood 122, 3918–3928 (2013).
CAS  PubMed  PubMed Central  Google Scholar 

75.
de Jong, J. L. & Zon, L. I. Use of the zebrafish system to study primitive and definitive hematopoiesis. Ann. Rev. Genet. 39, 481–501 (2005).
PubMed  Google Scholar 

76.
Athanasiadis, E. I. et al. Single-cell RNA-sequencing uncovers transcriptional states and fate decisions in haematopoiesis. Nat. Commun. 8, 2045 (2017).
PubMed  PubMed Central  Google Scholar 

77.
Zeng, A. et al. Prospectively isolated tetraspanin(+) neoblasts are adult pluripotent stem cells underlying planaria regeneration. Cell 173, 1593–1608 (2018).
CAS  PubMed  Google Scholar 

78.
Schindelin, J. et al. Fiji: an open-source platform for biological-image analysis. Nat. Methods 9, 676–682 (2012).
CAS  Google Scholar 

79.
Sun, K. et al. Endotrophin triggers adipose tissue fibrosis and metabolic dysfunction. Nat. Commun. 5, 3485 (2014).
PubMed  PubMed Central  Google Scholar 

80.
R Core Team R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2014).

81.
Benjamini, Y. & Hochberg, Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. R. Stat. Soc. B 57, 289–300 (1995).
Google Scholar  More

1.
Farquhar, J., Zerkle, A. L. & Bekker, A. in The Atmosphere – History 2nd edn, Vol. 6 (ed. Farquhar, J.) 91–138 (Elsevier, 2014).
2.
Lyons, T. W., Reinhard, C. T. & Planesky, N. J. The rise of oxygen in Earth’s early ocean and atmosphere. Nature 506, 307–315 (2014).
Google Scholar 

3.
Holland, H. D. Volcanic gases, black smokers and the great oxidation event. Geochim. Cosmochim. Acta 66, 3811–3826 (2002).
Google Scholar 

4.
Kump, L. R. & Barley, M. E. Increased subaerial volcanism and the rise of atmospheric oxygen 2.5 billion years ago. Nature 448, 1033–1036 (2007).
Google Scholar 

5.
Korenaga, J. Crustal evolution and mantle dynamics through Earth history. Philos. Trans. R. Soc. A 376, 2017048 (2018).
Google Scholar 

6.
Canfield, D. E. The early history of atmospheric oxygen: homage to Robert M. Garrels. Annu. Rev. Earth Planet. Sci. 33, 1–36 (2005).
Google Scholar 

7.
Holland, H. D. The oxygenation of the atmosphere and oceans. Philos. Trans. R. Soc. B. 363, 903–915 (2006).
Google Scholar 

8.
Gaillard, F., Scaillet, B. & Arndt, N. T. Atmospheric oxygenation caused by a change in volcanic degassing pressure. Nature 478, 228–232 (2011).
Google Scholar 

9.
Farquhar, J., Bao, H. M. & Thiemens, M. Atmospheric influence of Earth’s earliest sulfur cycle. Science 289, 756–758 (2000).
Google Scholar 

10.
Pavlov, A. A. & Kasting, J. F. Mass-independent fractionation of sulfur isotopes in Archean sediments: strong evidence for an anoxic Archean atmosphere. Astrobiology 2, 27–41 (2002).
Google Scholar 

11.
Symonds, R. B., Rose, W. I., Bluth, G. J. S. & Gerlach, T. M. in Volatiles in Magmas Vol. 30 (eds Caroll, M. R. & Halloway, J. R.) 1–66 (Mineralogical Society of America, 1994).

12.
Oppenheimer, C., Fischer, T. P. & Scaillet, B. in The Crust 2nd edn, Vol. 4 (ed. Rudnick, R. L.) 111–179 (Elsevier, 2014).

13.
National Academies of Sciences, Engineering and Medicine. Volcanic Eruptions and their Repose, Unrest, Precursors, and Timing (The National Academy Press, 2017).

14.
Drummond, S. E. Jr Boiling and Mixing of Hydrothermal Fluids: Chemical Effects on Mineral Precipitation. PhD thesis, Pennsylvania State Univ. (1981).

15.
German, C. R. & Von Damm, K. L. in The Oceans and Marine Geochemistry Vol. 6 (ed. Elderfield, H.) 181–222 (Elsevier, 2006).

16.
Giggenbach, W. F. Redox processes governing the chemistry of fumarolic gas discharges from White Island, New Zealand. Appl. Geochem. 2, 143–161 (1987).
Google Scholar 

17.
Lasaga, A. C. & Ohmoto, H. The oxygen geochemical cycle: dynamics and stability. Geochim. Cosmochim. Acta 66, 361–381 (2002).
Google Scholar 

18.
Ohmoto, H. in The Precambrian Earth: Tempos and Events Vol. 12 (eds Erickson, P. G. et. al.) 361–387 (Elsevier, 2004).

19.
Ohmoto, H. et al. Oxygen, iron and sulfur geochemical cycles on early Earth: paradigms and contradictions. Geol. Soc. Am. Spec. Pap. 504, 55–95 (2014).
Google Scholar 

20.
Burnham, C. W. & Ohmoto, H. in Granitic Magmatism and Related Mineralization Vol. 8 (eds. Ishihara, S. & Takenouchi, S.) 1–11 (1980).

21.
Berry, A. J. et al. A re-assessment of the oxidation state of iron in MORB glasses. Earth Planet. Sci. Lett. 483, 114–123 (2018).
Google Scholar 

22.
Carroll, M. R. & Webster, J. D. in Volatiles in Magmas Vol. 30 (eds Caroll, M. R. & Halloway, J. R.) 231–280 (Mineralogical Society of America, 1994).

23.
Carmichael, I. S. E. The redox states of basic and silicic magmas: a reflection of their source region? Contrib. Mineral. Petrol. 106, 129–141 (1991).
Google Scholar 

24.
Frost, D. J. & McCammon, C. A. The redox state of Earth’s mantle. Annu. Rev. Earth Planet. Sci. 36, 389–420 (2008).
Google Scholar 

25.
Evans, K. A. The redox budget of subduction zones. Earth Sci. Rev. 113, 11–32 (2012).
Google Scholar 

26.
Richards, J. P. The oxidation state, and sulfur and Cu contents of arc magmas: implications for metallurgy. Lithos 233, 27–45 (2015).
Google Scholar 

27.
Chappell, B. W. & White, A. J. R. Two contrasting granite types. Pac. Geol. 8, 173–174 (1974).
Google Scholar 

28.
Ishihara, S. The magnetite-series and ilmenite-series granitic rocks. Min. Geol. 27, 291–305 (1977).
Google Scholar 

29.
Savarino, J. et al. UV induced mass-independent sulfur isotope fractionation in stratospheric volcanic sulfate. Geophys. Res. Lett. 30, 2131 (2003).
Google Scholar 

30.
Hattori, S. et al. SO2 photoexcitation mechanism links mass-independent sulfur isotopic fractionation in cryospheric sulfate to climate impacting volcanism. Proc. Natl Acad. Sci. USA 110, 17661–17656 (2019).
Google Scholar 

31.
Whitehill, A. R., Jiang, B., Guo, H. & Ono, S. SO2 photolysis as a source for sulfur mass-independent isotope signatures in stratospheric aerosols. Atmos. Chem. Phys. 15, 1843–1864 (2015).
Google Scholar 

32.
Sasaki, A. & Ishihara, S. Sulfur isotopic composition of the magnetite-series and ilmenite-series granitoids in Japan. Contrib. Mineral. Petrol. 68, 107–115 (1979).
Google Scholar 

33.
Alt, J. C., Shanks, W. C. & Jackson, M. C. Cycling of sulfur in subduction zones: the geochemistry of sulfur in the Mariana Island Arc and back-arc trough. Earth Planet. Sci. Lett. 119, 477–494 (1993).
Google Scholar 

34.
Ohmoto, H. et al. Chemical processes of Kuroko formation. Econ. Geol. Mon. 5, 570–604 (1983).

35.
Ohmoto, H. Formation of volcanogenic massive sulfide deposits: the Kuroko perspective. Ore Geol. Rev. 10, 135–177 (1996).
Google Scholar 

36.
Ohmoto, H. & Goldhaber, M. B. in Geochemistry of Hydrothermal Ore Deposits 3rd edn (ed. Barnes, H. L.) 517–611 (Wiley, 1997).

37.
Kishima, N. A thermodynamic study on the pyrite–pyrrhotite–magnetite–water system at 300–500 °C with relevance to the fugacity/concentration quotient of aqueous H2S. Geochim. Cosmochim. Acta 53, 2143–2155 (1989).
Google Scholar 

38.
Schoonen, M. A. A. & Barnes, H. L. Mechanisms of pyrite and marcasite formation from solutions. III. Hydrothermal processes. Geochim. Cosmochim. Acta 55, 3491–3504 (1991).
Google Scholar 

39.
Graham, U. M. & Ohmoto, H. Experimental study of formation mechanisms of hydrothermal pyrite. Geochim. Cosmochim. Acta 58, 2187–2202 (1994).
Google Scholar 

40.
Kerrich, R. & Said, N. Extreme positive Ce anomalies in a 3.0 Ga submarine volcanic sequence, Murchison Province: oxygenated marine bottom waters. Chem. Geol. 280, 232–241 (2011).
Google Scholar 

41.
Kerrich, R., Said, N., Manikyamba, C. & Wyman, D. Sampling oxygenated Archean hydrosphere: implications from fractionations of Th/U and Ce/Ce* in hydrothermally altered volcanic sequences. Gondwana Res. 23, 506–525 (2013).
Google Scholar 

42.
van Keken, P. E., Kiefer, B. & Peacock, S. M. High-resolution models of subduction zones: implications for mineral dehydration reactions and the transport of water into the deep mantle. Geochem. Geophys. Geosyst. 3, 1056 (2002).
Google Scholar 

43.
Hyndman, R. D. & Peacock, S. M. Serpentinization of the forearc mantle. Earth Planet. Sci. Lett. 212, 417–432 (2003).
Google Scholar 

44.
Tomkins, A. G. & Evans, K. A. Separate zones of sulfate and sulfide release from subducted mafic oceanic crust. Earth Planet. Sci. Lett. 428, 73–83 (2015).
Google Scholar 

45.
Scaillet, B., Clemente, B., Evans, B. & Pichavant, M. Redox control of sulfur degassing in silicic magmas. J. Geophys. Res. 103, 23937–23949 (1998).
Google Scholar 

46.
Wallace, P. J. Volatiles in subduction zone magmas: concentrations and fluxes based on melt inclusions and volcanic gas data. J. Volcanol. 140, 217–240 (2005).
Google Scholar 

47.
Jugo, P. J. Sulfur content at sulfide saturation in oxidized magmas. Geology 37, 415–418 (2009).
Google Scholar 

48.
Ishihara, S. et al. in Evolution of Early Earth’s Atmosphere, Hydrosphere and Biosphere—Constraints from Ore Deposits Vol. 198 (eds Kesler, S. E. & Ohmoto, H.) 67–80 (Geological Society of America, 2006).

49.
Barboni, M. et al. Early formation of the Moon 4.51 billion years ago. Sci. Adv. 2017, 1602365 (2017).
Google Scholar 

50.
Delano, J. W. Redox history of the Earth’s interior since ~3,900 Ma: implications for prebiotic molecules. Orig. Life Evol. Biosphere 31, 311–341 (2001).
Google Scholar 

51.
Nicklas, R. W., Puchtel, I. S. & Ash, R. D. Redox state of the Archean mantle: evidence from V partitioning in 3.5–2.4 Ga komatiites. Geochim. Cosmochim. Acta 222, 447–446 (2018).
Google Scholar 

52.
Li, Z.-X. A. & Lee, C.-T. A. The constancy of upper mantle fO2 through time inferred from V/Sc ratios in basalts. Earth Planet. Sci. Lett. 228, 483–493 (2004).
Google Scholar 

53.
Trail, D., Watson, E. B. & Tailby, N. D. The oxidation state of Hadean magmas and implications for early Earth’s atmosphere. Nature 480, 79–83 (2011).
Google Scholar 

54.
Watanabe, Y., Farquhar, J. & Ohmoto, H. Anomalous fractionations of sulfur isotopes during thermochemical sulfate reduction. Science 324, 370–373 (2008).
Google Scholar 

55.
Oduro, H. et al. Evidence of magnetic isotope effects during thermochemical sulfate reduction. Proc. Natl Acad. Sci. USA 108, 17635–17638 (2011).
Google Scholar 

56.
Ohmoto et al. (Bio)geochemical cycles of S, C, Fe, and O on the hotter Archean Earth. Goldschmidt Abstr. 2018, abstr. 1913 (2018).

57.
Ohmoto, H., Watanabe, Y. & Kumazawa, K. Evidence from massive siderite beds for a CO2-rich atmosphere before ~1.8 billion years ago. Nature 429, 395–399 (2004).
Google Scholar 

58.
Finlayson-Pitts, B. J. & Pitts, J. N. Chemistry of the Upper and Lower Atmosphere (Academic Press, 1999).

59.
Seccombe, P. K. Sulphur isotope and trace metal composition of stratiform sulphides as an ore guide in the Canadian Shield. J. Geochem. Explor. 8, 117–137 (1977).
Google Scholar 

60.
Jamieson, J. W., Wing, B. A., Farquhar, J. & Hamington, M. D. Neoarchaean seawater sulphate concentrations from sulphur isotopes in massive sulphide ore. Nat. Geosci. 6, 61–64 (2013).
Google Scholar 

61.
Vaughan, D. J. & Craig, J. R. in Geochemistry of Hydrothermal Ore Deposits 2nd edn (ed. Barnes, H. L.) 367–434 (Wiley, 1979).

62.
Mysen, B. & Boettcher, A. L. Melting of a hydrous mantle. I. Phase relations of natural peridotite at high pressures and temperatures with controlled activities of water, carbon dioxide and hydrogen. J. Petrol. 16, 520–548 (1975).
Google Scholar 

63.
Gaetani, G. & Grove, T. L. The influence of water on melting of mantle peridotite. Contrib. Mineral. Petrol. 131, 323–346 (1998).
Google Scholar 

64.
Henderson, P. & Henderson, G. M. The Cambridge Handbook of Earth Science Data (Cambridge Univ. Press, 2009).

65.
Deines, P. & Harris, J. W. Sulfide inclusion chemistry and carbon isotopes of African diamonds. Geochim. Cosmochim. Acta 59, 3173–3188 (1995).
Google Scholar 

66.
Rudnick, R. L., Eldridge, C. S. & Bulanova, G. P. Diamond growth history from in situ measurement of Pb and S isotopic compositions of sulfide inclusions. Geology 21, 13–16 (1993).
Google Scholar 

67.
Farquhar, J. et al. Mass-independent sulfur of inclusions in diamond and sulfur recycling on early earth. Science 298, 2369–2371 (2002).
Google Scholar 

68.
Hickman, A. H. Review of the Pilbara Craton and Fortescue Basin, Western Australia: crustal evolution providing environments for early life. Isl. Arc 21, 1–31 (2012).
Google Scholar 

69.
van Kranendonk, M. J., Smithies, R. H., Hickman, A. H. & Champion, D. C. in Earth’s Oldest Rocks (eds van Kranendonk, M. J. et al.) 307–337 (Elsevier, 2007). More

1.
McFall-Ngai M, Hadfield MG, Bosch TCG, Carey HV, Domazet-Lošo T, Douglas AE, et al. Animals in a bacterial world, a new imperative for the life sciences. Proc Natl Acad Sci USA. 2013;110:3229–36.
CAS  PubMed  Google Scholar 
2.
Moran NA, Bennett GM. The tiniest tiny genomes. Annu Rev Microbiol. 2014;68:195–215.
CAS  PubMed  Google Scholar 

3.
Douglas AE. Multiorganismal insects: diversity and function of resident microorganisms. Annu Rev Entomol. 2015;60:17–34.
CAS  PubMed  Google Scholar 

4.
Engelstädter J, Hurst GDD. The ecology and evolution of microbes that manipulate host reproduction. Annu Rev Ecol Evol Syst. 2009;40:127–49.
Google Scholar 

5.
Ma WJ, Schwander T. Patterns and mechanisms in instances of endosymbiont-induced parthenogenesis. J Evol Biol. 2017;30:868–88.
PubMed  Google Scholar 

6.
Bondy EC, Hunter MS. Sex ratios in the haplodiploid herbivores, aleyrodidae and thysanoptera: a review and tools for study. Adv Insect Physiol. 2019;56:251–81.
Google Scholar 

7.
Hunter MS, Perlman SJ, Kelly SE. A bacterial symbiont in the Bacteroidetes induces cytoplasmic incompatibility in the parasitoid wasp Encarsia pergandiella. Proc Natl Acad Sci USA. 2003;270:2185–90.
Google Scholar 

8.
Beckmann JF, Ronau JA, Hochstrasser MA. Wolbachia deubiquitylating enzyme induces cytoplasmic incompatibility. Nat Microbiol 2017;2:17007.
PubMed  PubMed Central  Google Scholar 

9.
Harumoto T, Lemaitre B. Male-killing toxin in a bacterial symbiont of Drosophila. Nature 2018;557:252–5.
CAS  PubMed  PubMed Central  Google Scholar 

10.
Hosokawa T, Koga R, Kikuchi Y, Meng XY, Fukatsu T. Wolbachia as a bacteriocyte-associated nutritional mutualist. Proc Natl Acad Sci USA. 2010;107:769–74.
CAS  PubMed  Google Scholar 

11.
Michalkova V, Benoit JB, Weiss BL, Attardo GM, Aksoy S. Vitamin B6 generated by obligate symbionts is critical for maintaining proline homeostasis and fecundity in tsetse flies. Appl Environ Microbiol. 2014;80:5844–53.
PubMed  PubMed Central  Google Scholar 

12.
Moriyama M, Nikoh N, Hosokawa T, Fukatsu T. Riboflavin provisioning underlies Wolbachia’s fitness contribution to its insect host. mBio . 2015;6:e01732–15.
CAS  PubMed  PubMed Central  Google Scholar 

13.
Snyder AK, Rio RVM. ‘Wigglesworthia morsitans’ folate (vitamin B9) biosynthesis contributes to tsetse host fitness. Appl Environ Microbiol. 2015;81:5375–86.
CAS  PubMed  PubMed Central  Google Scholar 

14.
Ju JF, Bing XL, Zhao DS, Guo Y, Xi Z, Hoffmann AA, et al. Wolbachia supplement biotin and riboflavin to enhance reproduction in planthoppers. ISME J. 2019;14:676–87.
PubMed  Google Scholar 

15.
Tsuchida T, Koga R, Shibao H, Matsumoto T, Fukatsu T. Diversity and geographic distribution of secondary endosymbiotic bacteria in natural populations of the pea aphid, Acyrthosiphon pisum. Mol Ecol. 2002;11:2123–35.
CAS  PubMed  Google Scholar 

16.
Baumann P. Biology of bacteriocyte-associated endosymbionts of plant sap-sucking insects. Annu Rev Microbiol. 2005;59:155–89.
CAS  PubMed  PubMed Central  Google Scholar 

17.
Gottlieb Y, Ghanim M, Gueguen G, Kontsedalov S, Vavre F, Fleury F, et al. Inherited intracellular ecosystem: symbiotic bacteria share bacteriocytes in whiteflies. FASEB J. 2008;22:2591–9.
CAS  PubMed  Google Scholar 

18.
Sloan DB, Moran NA. Genome reduction and co-evolution between the primary and secondary bacterial symbionts of psyllids. Mol Biol Evol. 2012;29:3781–92.
CAS  PubMed  PubMed Central  Google Scholar 

19.
Skaljac M, Zanic K, Ban SG, Kontsedalov S, Ghanim M. Co-infection and localization of secondary symbionts in two whitefly species. BMC Microbiol. 2010;10:142.
PubMed  PubMed Central  Google Scholar 

20.
McCutcheon JP, Von Dohlen CD. An interdependent metabolic patchwork in the nested symbiosis of mealybugs. Curr Biol. 2011;21:1366–72.
CAS  PubMed  PubMed Central  Google Scholar 

21.
Husnik F, Nikoh N, Koga R, Ross L, Duncan RP, Fujie M, et al. Horizontal gene transfer from diverse bacteria to an insect genome enables a tripartite nested mealybug symbiosis. Cell. 2013;153:1567–78.
CAS  PubMed  Google Scholar 

22.
Koga R, Meng XY, Tsuchida T, Fukatsu T. Cellular mechanism for selective vertical transmission of an obligate insect symbiont at the bacteriocyte-embryo interface. Proc Natl Acad Sci USA. 2012;109:E1230–E1237.
CAS  PubMed  Google Scholar 

23.
Fukatsu T, Nikoh N. Two intracellular symbiotic bacteria from the mulberry psyllid Anomoneura mori (Insecta, Homoptera). Appl Environ Microbiol. 1998;64:3599–606.
CAS  PubMed  PubMed Central  Google Scholar 

24.
Degnan PH, Yu Y, Sisneros N, Wing RA, Moran NA. Hamiltonella defensa, genome evolution of protective bacterial endosymbiont from pathogenic ancestors. Proc Natl Acad Sci USA. 2009;106:9063–8.
CAS  PubMed  Google Scholar 

25.
Rao Q, Wang S, Su YL, Bing XL, Liu SS, Wang XW. Draft genome sequence of ‘Candidatus Hamiltonella defensa’ an endosymbiont of the whitefly Bemisia tabaci. J Bacteriol. 2012;194:3558.
CAS  PubMed  PubMed Central  Google Scholar 

26.
Xue J, Zhou X, Zhang CX, Yu LL, Fan HW, Wang Z, et al. Genomes of the rice pest brown planthopper and its endosymbionts reveal complex complementary contributions for host adaptation. Genome Biol. 2014;15:521.
PubMed  PubMed Central  Google Scholar 

27.
Santos-Garcia D, Juravel K, Freilich S, Zchori-Fein E, Latorre A, Moya A, et al. To B or not to B: comparative genomics suggests Arsenophonus as a source of B vitamins in whiteflies. Front Microbiol. 2018;9:2254–70.
PubMed  PubMed Central  Google Scholar 

28.
Ouvrard D, Martin JH. The whiteflies: taxonomic checklist of the world’s whiteflies (Insecta: Hemiptera: Aleyrodidae). 2019. http://www.hemiptera-databases.org/whiteflies/.

29.
Yang P. The greenhouse whiteflies and plant quarantine. Chin Bull Entomol. 1981;18:69–71.
Google Scholar 

30.
Liu SS, De Barro PJ, Xu J, Luan JB, Zang LS, Ruan YM, et al. Asymmetric mating interactions drive widespread invasion and displacement in a whitefly. Science . 2007;318:1769–72.
CAS  PubMed  Google Scholar 

31.
Zchori-Fein E, Lahav T, Freilich S. Variations in the identity and complexity of endosymbiont combinations in whitefly hosts. Front Microbiol. 2014;5:310.
PubMed  PubMed Central  Google Scholar 

32.
Luan JB, Shan HW, Isermann P, Huang JH. Cellular and molecular remodelling of a host cell for vertical transmission of bacterial symbionts. Proc R Soc B. 2016;283:20160580.
PubMed  Google Scholar 

33.
Luan JB, Sun XP, Fei ZJ, Douglas AE. Maternal inheritance of a single somatic animal cell displayed by the bacteriocyte in the whitefly Bemisia tabaci. Curr Biol. 2018;28:459–65.
CAS  PubMed  PubMed Central  Google Scholar 

34.
Shan HW, Luan JB, Liu YQ, Douglas AE, Liu SS. The inherited bacterial symbiont Hamiltonella influences the sex ratio of an insect host. Proc R Soc B. 2019;286:20191677.
CAS  PubMed  Google Scholar 

35.
Rao Q, Rollat-Farnier PA, Zhu DT, Santos-Garcia D, Silva FJ, Moya A, et al. Genome reduction and potential metabolic complementation of the dual endosymbionts in the whitefly Bemisia tabaci. BMC Genom. 2015;16:226.
Google Scholar 

36.
Scott IAW, Workman PJ, Drayton GM, Burnip GM. First record of Bemisia tabaci biotype Q in New Zealand. N Z Plant Prot. 2007;60:264–70.
CAS  Google Scholar 

37.
Qin L, Pan LL, Liu SS. Further insight into reproductive incompatibility between putative cryptic species of the Bemisia tabaci whitefly complex. Insect Sci. 2016;23:215–24.
CAS  PubMed  Google Scholar 

38.
Xu XR, Li NN, Bao XY, Douglas AE, Luan JB. Patterns of host cell inheritance in the bacterial symbiosis of whiteflies. Insect Sci. 2019; https://doi.org/10.1111/1744-7917.12708.

39.
Schmittgen TD, Livak KJ. Analyzing real-time PCR data by the comparative CT method. Nat Protoc. 2008;3:1101–8.
CAS  PubMed  Google Scholar 

40.
Gottlieb Y, Ghanim M, Chiel E, Gerling D, Portnoy V, Steinberg S, et al. Identification and localization of a Rickettsia sp. in Bemisia tabaci (Homoptera: Aleyrodidae). Appl Environ Microbiol. 2006;72:3646–52.
CAS  PubMed  PubMed Central  Google Scholar 

41.
Hadjistylli M, Schwartz SA, Brown JK, Roderick GK. Isolation and characterization of nine microsatellite loci from Bemisia tabaci (Hemiptera: Aleyrodidae) biotype B. J Insect Sci. 2014;14:148.
CAS  PubMed  PubMed Central  Google Scholar 

42.
Bondy EC, Hunter MS. Determining the egg fertilization rate of Bemisia tabaci using a cytogenetic technique. J Vis Exp. 2019;https://doi.org/10.3791/59213.

43.
Ankrah NYD, Luan JB, Douglasa AE. Cooperative metabolism in a three-partner insect-bacterial symbiosis revealed by metabolic modeling. J Bacteriol 2017;199:e00872–16.
CAS  PubMed  PubMed Central  Google Scholar 

44.
Ren FR, Bai B, Hong JS, Huang YZ, Luan JB. A microbiological assay for biotin determination in insects. Insect Sci. 2020; https://doi.org/10.1111/1744-7917.12827.

45.
Salem H, Bauer E, Strauss AS, Vogel H, Marz M, Kaltenpoth M. Vitamin supplementation by gut symbionts ensures metabolic homeostasis in an insect host. Proc R Soc B. 2014;281:1838.
Google Scholar 

46.
Duron O, Morel O, Noël V, Buysse M, Binetruy F, Lancelot R, et al. Tick-bacteria mutualism depends on B vitamin synthesis pathways. Curr Biol. 2018;28:1896–902.
CAS  PubMed  Google Scholar 

47.
Pant NC, Fraenkel G. The function of the symbiotic yeasts of two insect species, Lasioderma serricorne F. and Stegobium (Sitodrepa) paniceum L. Science. 1950;112:498–500.
CAS  PubMed  Google Scholar 

48.
Byrne DN, Bellows TS Jr. Whitefly biology. Annu Rev Entomol. 1991;36:431–57.
Google Scholar 

49.
Giorgini M, Monti MM, Caprio E, Stouthamer R, Hunter MS. Feminization and the collapse of haplodiploidy in an asexual parasitoid wasp harboring the bacterial symbiont Cardinium. Heredity. 2009;102:365–71.
CAS  PubMed  Google Scholar 

50.
Ma WJ, Pannebakker BA, van de Zande L, Schwander T, Wertheim B, Beukeboom LW. Diploid males support a two-step mechanism of endosymbiont-induced thelytoky in a parasitoid wasp. BMC Evol Biol. 2015;15:84.
PubMed  PubMed Central  Google Scholar 

51.
Sloan DB, Moran NA. The evolution of genomic instability in the obligate endosymbionts of whiteflies. Genome Biol Evol. 2013;5:783–93.
PubMed  PubMed Central  Google Scholar 

52.
Chen W, Hasegawa DK, Kaur N, Kliot A, Pinheiro PV, Luan JB, et al. The draft genome of whitefly Bemisia tabaci MEAM1, a global crop pest, provides novel insights into virus transmission, host adaptation, and insecticide resistance. BMC Biol. 2016;14:110.
PubMed  PubMed Central  Google Scholar 

53.
Luan JB, Chen W, Hasegawa DK, Simmons A, Wintermantel WM, Ling KS, et al. Metabolic coevolution in the bacterial symbiosis of whiteflies and related plant sap-feeding insects. Genome Biol Evol. 2015;7:2635–47.
CAS  PubMed  PubMed Central  Google Scholar 

54.
Russell JA, Latorre A, Sabater-Muñoz B, Moya A, Moran NA. Side-stepping secondary symbionts: widespread horizontal transfer across and beyond the Aphidoidea. Mol Ecol. 2003;12:1061–75.
CAS  PubMed  Google Scholar 

55.
Manzano-Marı́n A, Coeur d’acier A, Clamens AL, Orvain C, Cruaud C, Barbe V, et al. Serial horizontal transfer of vitamin-biosynthetic genes enables the establishment of new nutritional symbionts in aphids’ di-symbiotic systems. ISME J. 2020;14:259–73.
Google Scholar 

56.
Ayoubi A, Talebi AA, Fathipour Y, Mehrabadi M. Coinfection of the secondary symbionts, Hamiltonella defensa and Arsenophonus sp. contribute to the performance of the major aphid pest, Aphis gossypii (Hemiptera: Aphididae). Insect Sci. 2020;27:86–98.
PubMed  Google Scholar 

57.
Thao MLL, Baumann P. Evidence for multiple acquisition of Arsenophonus by whitefly species (Sternorrhyncha: Aleyrodidae). Curr Microbiol. 2004;48:140–4.
CAS  PubMed  Google Scholar 

58.
Nováková E, Hypša V, Moran NA. Arsenophonus, an emerging clade of intracellular symbionts with a broad host distribution. BMC Microbiol. 2009;9:143.
PubMed  PubMed Central  Google Scholar 

59.
Nováková E, Husník F, Šochová E, Hypša V. Arsenophonus and Sodalis symbionts in louse flies: an analogy to the Wigglesworthia and Sodalis system in tsetse flies. Appl Environ Microbiol. 2015;81:6189–99.
PubMed  PubMed Central  Google Scholar 

60.
Nikoh N, Hosokawa T, Moriyama M, Oshima K, Hattori M, Fukatsu T. Evolutionary origin of insect-Wolbachia nutritional mutualism. Proc Natl Acad Sci USA. 2014;111:10257–62.
CAS  PubMed  Google Scholar 

61.
Wu D, Daugherty SC, Van Aken SE, Pai GH, Watkins KL, Khouri H, et al. Metabolic complementarity and genomics of the dual bacterial symbiosis of sharpshooters. PLoS Biol. 2006;4:e188.
PubMed  PubMed Central  Google Scholar 

62.
McCutcheon JP, Moran NA. Parallel genomic evolution and metabolic interdependence in an ancient symbiosis. Proc Natl Acad Sci USA. 2007;104:19392–7.
CAS  PubMed  Google Scholar 

63.
McCutcheon JP, McDonald BR, Moran NA. Convergent evolution of metabolic roles in bacterial co-symbionts of insects. Proc Natl Acad Sci USA. 2009;106:15394–9.
CAS  PubMed  Google Scholar 

64.
Matsuura Y, Moriyama M, Łukasik P, Vanderpool D, Tanahashi M, Meng XY, et al. Recurrent symbiont recruitment from fungal parasites in cicadas. Proc Natl Acad Sci USA. 2018;115:E5970–E5979.
CAS  PubMed  Google Scholar 

65.
Kapantaidaki DE, Ovcarenko I, Fytrou N, Knott KE, Bourtzis K, Tsagkarakou A. Low levels of mitochondrial DNA and symbiont diversity in the worldwide agricultural pest, the greenhouse whitefly Trialeurodes vaporariorum (Hemiptera: Aleyrodidae). J Hered. 2014;106:80–92.
PubMed  Google Scholar 

66.
Douglas AE. The B vitamin nutrition of insects: the contributions of diet, microbiome and horizontally acquired genes. Curr Opin Insect Sci. 2017;23:65–69.
PubMed  Google Scholar 

67.
Smykal V, Raikhel AS. Nutritional control of insect reproduction. Curr Opin Insect Sci. 2015;11:31–38.
PubMed  PubMed Central  Google Scholar 

68.
Wheeler D. The role of nourishment in oogenesis. Ann Rev Entomol. 1996;41:407–31.
CAS  Google Scholar 

69.
Himler AG, Adachi-Hagimori T, Bergen JE, Kozuch A, Kelly SE, Tabashnik BE, et al. Rapid spread of a bacterial symbiont in an invasive whitefly is driven by fitness benefits and female bias. Science. 2011;332:254–6.
CAS  PubMed  Google Scholar  More

1.
Ponomarova O, Patil KR. Metabolic interactions in microbial communities: untangling the Gordian knot. Curr Opin Microbiol. 2015;27:37–44.
PubMed  Google Scholar 
2.
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  Google Scholar 

3.
Schink B. Energetics of syntrophic cooperation in methanogenic degradation. Microbiol Mol Biol Rev. 1997;61:262–80.
CAS  PubMed  PubMed Central  Google Scholar 

4.
Pernthaler A, Dekas AE, Brown CT, Goffredi SK, Embaye T, Orphan VJ. Diverse syntrophic partnerships from deep-sea methane vents revealed by direct cell capture and metagenomics. Proc Natl Acad Sci USA. 2008;105:7052–7.
CAS  PubMed  Google Scholar 

5.
Men Y, Feil H, Verberkmoes NC, Shah MB, Johnson DR, Lee PKH, et al. Sustainable syntrophic growth of Dehalococcoides ethenogenes strain 195 with Desulfovibrio vulgaris Hildenborough and Methanobacterium congolense: global transcriptomic and proteomic analyses. ISME J. 2012;6:410–21.
CAS  PubMed  Google Scholar 

6.
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  Google Scholar 

7.
Marchal M, Goldschmidt F, Derksen-Müller SN, Panke S, Ackermann M, Johnson DR. A passive mutualistic interaction promotes the evolution of spatial structure within microbial populations. BMC Evol Biol. 2017;17:106.
PubMed  PubMed Central  Google Scholar 

8.
Thompson AW, Foster RA, Krupke A, Carter BJ, Musat N, Vaulot D, et al. Unicellular cyanobacterium symbiotic with a single-celled eukaryotic alga. Science. 2012;337:1546–50.
CAS  PubMed  Google Scholar 

9.
Zengler K, Palsson BO. A road map for the development of community systems (CoSy) biology. Nat Rev Microbiol. 2012;10:366–72.
CAS  PubMed  Google Scholar 

10.
Sachs JL, Hollowell AC. The origins of cooperative bacterial communities. MBio. 2012;3:1–3.

11.
Johnson DR, Goldschmidt F, Lilja EE, Ackermann M. Metabolic specialization and the assembly of microbial communities. ISME J. 2012;6:1985–91.
CAS  PubMed  PubMed Central  Google Scholar 

12.
Bull JJ, Rice WR. Distinguishing mechanisms for the evolution of co-operation. J Theor Biol. 1991;149:63–74.
CAS  PubMed  Google Scholar 

13.
Foster KR, Wenseleers T. A general model for the evolution of mutualisms. J Evol Biol. 2006;19:1283–93.
CAS  PubMed  Google Scholar 

14.
Weber KA, Achenbach LA, Coates JD. Microorganisms pumping iron: anaerobic microbial iron oxidation and reduction. Nat Rev Microbiol. 2006;4:752–64.
CAS  PubMed  Google Scholar 

15.
Lüdecke C, Reiche M, Eusterhues K, Nietzsche S, Küsel K. Acid-tolerant microaerophilic Fe(II)-oxidizing bacteria promote Fe(III)-accumulation in a fen. Environ Microbiol. 2010;12:2814–25.
PubMed  Google Scholar 

16.
Emerson D, Fleming EJ, McBeth JM. Iron-oxidizing bacteria: an environmental and genomic perspective. Annu Rev Microbiol. 2010;64:561–83.
CAS  PubMed  Google Scholar 

17.
Emerson D, Field EK, Chertkov O, Davenport KW, Goodwin L, Munk C, et al. Comparative genomics of freshwater Fe-oxidizing bacteria: implications for physiology, ecology, and systematics. Front Microbiol. 2013;4:254.
PubMed  PubMed Central  Google Scholar 

18.
Fabisch M, Beulig F, Akob DM, Küsel K. Surprising abundance of Gallionella-related iron oxidizers in creek sediments at pH 4.4 or at high heavy metal concentrations. Front Microbiol. 2013;4:390.
PubMed  PubMed Central  Google Scholar 

19.
Fleming EJ, Cetinić I, Chan CS, Whitney King D, Emerson D. Ecological succession among iron-oxidizing bacteria. ISME J. 2014;8:804–15.
CAS  PubMed  Google Scholar 

20.
Byrne JM, van der Laan G, Figueroa AI, Qafoku O, Wang C, Pearce CI, et al. Size dependent microbial oxidation and reduction of magnetite nano- and micro-particles. Sci Rep. 2016;6:1–13.
Google Scholar 

21.
Byrne JM, Klueglein N, Pearce C, Rosso KM, Appel E, Kappler A. Redox cycling of Fe(II) and Fe(III) in magnetite by Fe-metabolizing bacteria. Science. 2015;347:1473–6.

22.
Braunschweig J, Bosch J, Meckenstock RU. Iron oxide nanoparticles in geomicrobiology: from biogeochemistry to bioremediation. N. Biotechnol. 2013;30:793–802.
CAS  PubMed  Google Scholar 

23.
Bosch J, Heister K, Hofmann T, Meckenstock RU. Nanosized iron oxide colloids strongly enhance microbial iron reduction. Appl Environ Microbiol. 2010;76:184–9.
CAS  PubMed  Google Scholar 

24.
Küsel K, Blöthe M, Schulz D, Reiche M, Drake HL. Microbial reduction of iron and porewater biogeochemistry in acidic peatlands. Biogeosci Discuss. 2008;5:2165–96.
Google Scholar 

25.
Marsili E, Baron DB, Shikhare ID, Coursolle D, Gralnick JA, Bond DR. Shewanella secretes flavins that mediate extracellular electron transfer. Proc Natl Acad Sci USA. 2008;105:3968–73.
CAS  PubMed  Google Scholar 

26.
Royer RA, Burgos WD, Fisher AS, Unz RF, Dempsey BA. Enhancement of biological reduction of hematite by electron shuttling and Fe(II) complexation. Environ Sci Technol. 2002;36:1939–46.
CAS  PubMed  Google Scholar 

27.
Beckwith CR, Edwards MJ, Lawes M, Shi L, Butt JN, Richardson DJ, et al. Characterization of MtoD from Sideroxydans lithotrophicus: a cytochrome c electron shuttle used in lithoautotrophic growth. Front Microbiol. 2015;6:332.
PubMed  PubMed Central  Google Scholar 

28.
Hartshorne RS, Reardon CL, Ross D, Nuester J, Clarke TA, Gates AJ, et al. Characterization of an electron conduit between bacteria and the extracellular environment. Proc Natl Acad Sci USA. 2009;106:22169–74.
CAS  PubMed  Google Scholar 

29.
White GF, Shi Z, Shi L, Wang Z, Dohnalkova AC, Marshall MJ, et al. Rapid electron exchange between surface-exposed bacterial cytochromes and Fe(III) minerals. Proc Natl Acad Sci USA. 2013;110:6346–51.
CAS  PubMed  Google Scholar 

30.
Venkateswaran K, Moser DP, Dollhopf ME, Lies DP, Saffarini DA, MacGregor BJ, et al. Polyphasic taxonomy of the genus Shewanella and description of Shewanella oneidensis sp. nov. Int J Syst Bacteriol. 1999;49:705–24.
CAS  PubMed  Google Scholar 

31.
Myers CR, Nealson KH. Bacterial manganese reduction and growth with manganese oxide as the sole electron acceptor. Science. 1988;240:1319–21.
CAS  PubMed  Google Scholar 

32.
Myers CR, Nealson KH. Respiration-linked proton translocation coupled to anaerobic reduction of manganese(IV) and iron(III) in Shewanella putrefaciensMR-1. J Bacteriol. 1990;172:6232–8.
CAS  PubMed  PubMed Central  Google Scholar 

33.
McBeth JM, Little BJ, Ray RI, Farrar KM, Emerson D. Neutrophilic iron-oxidizing ‘Zetaproteobacteria’ and mild steel corrosion in nearshore marine environments. Appl Environ Microbiol. 2011;77:1405–12.
CAS  PubMed  Google Scholar 

34.
Mori JF, Ueberschaar N, Lu S, Cooper RE, Pohnert G, Küsel K. Sticking together: inter-species aggregation of bacteria isolated from iron snow is controlled by chemical signaling. ISME J. 2017;11:1075–86.
CAS  PubMed  PubMed Central  Google Scholar 

35.
Tamura H, Goto K, Yotsuyanagi T, Nagayama M. Spectrophotometric determination of iron(II) with 1,10-phenanthroline in the presence of large amounts of iron(III). Talanta. 1974;21:314–8.
CAS  PubMed  Google Scholar 

36.
Cooper RE, Wegner C-E, McAllister SM, Shevchenko O, Chan CS, Küsel K. Draft genome sequence of Sideroxydanssp. Strain CL21, an Fe(II)-oxidizing bacterium. Microbiol Resour Announc. 2020;9:1–2.

37.
Wegner C-E, Gaspar M, Geesink P, Herrmann M, Marz M, Küsel K. Biogeochemical regimes in shallow aquifers reflect the metabolic coupling of the elements nitrogen, sulfur, and carbon. Appl Environ Microbiol. 2019;8:1–19.

38.
Andrews S. FastQC: a quality control tool for high throughput sequence data. http://www.bioinformatics.babraham.ac.uk/projects/fastqc..40.

39.
Bushnell B. BBMap short read aligner. https://www.sourceforge.net/projects/bbmap/..41.

40.
Kopylova E, Noé L, Touzet H, Noe L, Touzet H. SortMeRNA: fast and accurate filtering of ribosomal RNAs in metatranscriptomic data. Bioinformatics. 2012;28:3211–7.
CAS  PubMed  Google Scholar 

41.
Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, et al. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res. 2013;41:D590–6.
CAS  PubMed  Google Scholar 

42.
Burge SW, Daub J, Eberhardt R, Tate J, Barquist L, Nawrocki EP, et al. Rfam 11.0: 10 years of RNA families. Nucleic Acids Res. 2013;41:D226–32.
CAS  PubMed  Google Scholar 

43.
Heidelberg JF, Paulsen IT, Nelson KE, Gaidos EJ, Nelson WC, Read TD, et al. Genome sequence of the dissimilatory metal ion-reducing bacterium Shewanella oneidensis. Nat Biotechnol. 2002;20:1118–23.
CAS  PubMed  Google Scholar 

44.
Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, et al. The sequence alignment/map format and SAM tools. Bioinformatics. 2009;25:2078–9.
PubMed  PubMed Central  Google Scholar 

45.
Liao Y, Smyth GK, Shi W. The Subread aligner: fast, accurate and scalable read mapping by seed-and-vote. Nucleic Acids Res. 2013;41:e108.
PubMed  PubMed Central  Google Scholar 

46.
Liao Y, Smyth GK, Shi W. featureCounts: an efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics. 2014;30:923–30.
CAS  Google Scholar 

47.
R Core Team. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. 2018.

48.
Robinson MD, McCarthy DJ, Smyth GK. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics. 2010;26:139–40.
CAS  Google Scholar 

49.
Tautenhahn R, Patti GJ, Rinehart D, Siuzdak G. XCMS Online: a web-based platform to process untargeted metabolomic data. Anal Chem. 2012;84:5035–9.
CAS  PubMed  PubMed Central  Google Scholar 

50.
Stettin D, Poulin RX, Pohnert G. Metabolomics benefits fom orbitrap GC-MS—Comparison of low- and high-resolution GC-MS. Metabolites. 2020;10:1–16.
Google Scholar 

51.
Chong J, Yamamoto M, Xia J. MetaboAnalystR 2.0: from raw spectra to biological insights. Metabolites. 2019;9:1–10.

52.
Hummel J, Strehmel N, Bölling C, Schmidt S, Walther D, Kopka J. Mass Spectral search and analysis using the golm metabolome database. In: Weckwerth W, Kahl G (eds). The handbook of plant metabolomics. 2013. Wiley-VCH Verlag GmbH & Co. KGaA, Weinheim, Germany, p. 321–43.

53.
Lueder U, Druschel G, Emerson D, Kappler A, Schmidt C. Quantitative analysis of O2 and Fe2+ profiles in gradient tubes for cultivation of microaerophilic Iron(II)-oxidizing bacteria. FEMS Microbiol Ecol. 2018;94:1–15.

54.
Lefevre E, Bossa N, Wiesner MR, Gunsch CK. A review of the environmental implications of in situ remediation by nanoscale zero valent iron (nZVI): behavior, transport and impacts on microbial communities. Sci Total Environ. 2016;565:889–901.
CAS  PubMed  PubMed Central  Google Scholar 

55.
Kirschling TL, Gregory KB, Minkley EG Jr, Lowry GV, Tilton RD. Impact of nanoscale zero valent iron on geochemistry and microbial populations in trichloroethylene contaminated aquifer materials. Environ Sci Technol. 2010;44:3474–80.
CAS  PubMed  Google Scholar 

56.
Wu S, Cajthaml T, Semerád J, Filipová A, Klementová M, Skála R, et al. Nano zero-valent iron aging interacts with the soil microbial community: a microcosm study. Environ Sci: Nano. 2019;6:1189–206.
CAS  Google Scholar 

57.
Auffan M, Rose J, Wiesner MR, Bottero J-Y. Chemical stability of metallic nanoparticles: a parameter controlling their potential cellular toxicity in vitro. Environ Pollut. 2009;157:1127–33.
CAS  Google Scholar 

58.
Anza M, Salazar O, Epelde L, Alkorta I, Garbisu C. The application of nanoscale zero-valent iron promotes soil remediation while negatively affecting soil microbial biomass and activity. Front Environ Sci. 2019;7:1–6.
Google Scholar 

59.
Friedrich B, Magasanik B. Enzymes of agmatine degradation and the control of their synthesis in Klebsiella aerogenes. J Bacteriol. 1979;137:1127–33.
CAS  PubMed  PubMed Central  Google Scholar 

60.
Kurihara S, Oda S, Kato K, Kim HG, Koyanagi T, Kumagai H, et al. A novel putrescine utilization pathway involves gamma-glutamylated intermediates of Escherichia coli K-12. J Biol Chem. 2005;280:4602–8.
CAS  PubMed  Google Scholar 

61.
Hädrich A, Taillefert M, Akob DM, Cooper RE, Litzba U, Wagner FE, et al. Microbial Fe(II) oxidation by Sideroxydans lithotrophicus ES-1 in the presence of Schlöppnerbrunnen fen-derived humic acids. FEMS Microbiol Ecol. 2019;95:1–19.

62.
Cooper RE, Eusterhues K, Wegner C-E, Totsche KU, Küsel K. Ferrihydrite-associated organic matter (OM) stimulates reduction by Shewanella oneidensis MR-1 and a complex microbial consortia. Biogeosciences. 2017;14:5171–88.
CAS  Google Scholar 

63.
Liu J, Wang Z, Belchik SM, Edwards MJ, Liu C, Kennedy DW, et al. Identification and characterization of MtoA: a decaheme c-type cytochrome of the neutrophilic Fe(II)-oxidizing bacterium Sideroxydans lithotrophicus ES-1. Front Microbiol. 2012;3:37.
CAS  PubMed  PubMed Central  Google Scholar 

64.
DiChristina TJ, Moore CM, Haller CA. Dissimilatory Fe(III) and Mn(IV) reduction by Shewanella putrefaciens requires ferE, a homolog of the pulE (gspE) type II protein secretion gene. J Bacteriol. 2002;184:142–51.
CAS  PubMed  PubMed Central  Google Scholar 

65.
Meshulam-Simon G, Behrens S, Choo AD, Spormann AM. Hydrogen metabolism in Shewanella oneidensis MR-1. Appl Environ Microbiol. 2007;73:1153–65.
CAS  PubMed  Google Scholar 

66.
Shi L, Belchik SM, Plymale AE, Heald S, Dohnalkova AC, Sybirna K, et al. Purification and characterization of the [NiFe]-hydrogenase of Shewanella oneidensis MR-1. Appl Environ Microbiol. 2011;77:5584–90.
CAS  PubMed  PubMed Central  Google Scholar 

67.
Vignais PM, Billoud B, Meyer J. Classification and phylogeny of hydrogenases. FEMS Microbiol Rev. 2001;25:455–501.
CAS  PubMed  Google Scholar 

68.
Reiche M, Torburg G, Küsel K. Competition of Fe(III) reduction and methanogenesis in an acidic fen. FEMS Microbiol Ecol. 2008;65:88–101.
CAS  PubMed  Google Scholar 

69.
Reiche M, Haedrich A, Lischeid G, Kuesel K, Hädrich A, Lischeid G, et al. Impact of manipulated drought and heavy rainfall events on peat mineralization processes and source-sink functions of an acidic fen. J Geophys Res-Biogeosci. 2009;114:1–13.
Google Scholar 

70.
Hädrich A, Heuer VB, Herrmann M, Hinrichs K-U, Küsel K. Origin and fate of acetate in an acidic fen. FEMS Microbiol Ecol. 2012;81:339–54.
PubMed  Google Scholar 

71.
Hamberger A, Horn MA, Dumont MG, Murrell JC, Drake HL. Anaerobic consumers of monosaccharides in a moderately acidic fen. Appl Environ Microbiol. 2008;74:3112–20.
CAS  PubMed  PubMed Central  Google Scholar 

72.
Wüst PK, Horn MA, Drake HL. Trophic links between fermenters and methanogens in a moderately acidic fen soil. Environ Microbiol. 2009;11:1395–409.
PubMed  Google Scholar 

73.
Tabor CW, Tabor H. Polyamines. Annu Rev Biochem. 1984;53:749–90.
CAS  PubMed  Google Scholar 

74.
Karatan E, Watnick P. Signals, regulatory networks, and materials that build and break bacterial biofilms. Microbiol Mol Biol Rev. 2009;73:310–47.
CAS  PubMed  PubMed Central  Google Scholar 

75.
Bachrach U, Heimer YM. The physiology of polyamines. 1989. CRC Press Taylor and Francis Group, Boca Raton, FL, USA.

76.
Karatan E, Duncan TR, Watnick PI. NspS, a predicted polyamine sensor, mediates activation of Vibrio cholerae biofilm formation by norspermidine. J Bacteriol. 2005;187:7434–43.
CAS  PubMed  PubMed Central  Google Scholar 

77.
Cockerell SR, Rutkovsky AC, Zayner JP, Cooper RE, Porter LR, Pendergraft SS, et al. Vibrio cholerae NspS, a homologue of ABC-type periplasmic solute binding proteins, facilitates transduction of polyamine signals independent of their transport. Microbiology. 2014;160:832–43.
CAS  PubMed  PubMed Central  Google Scholar 

78.
Matthysse AG, Yarnall HA, Young N. Requirement for genes with homology to ABC transport systems for attachment and virulence of Agrobacterium tumefaciens. J Bacteriol. 1996;178:5302–8.
CAS  PubMed  PubMed Central  Google Scholar 

79.
Sauer K, Camper AK. Characterization of phenotypic changes in Pseudomonas putida in response to surface-associated growth. J Bacteriol. 2001;183:6579–89.
CAS  PubMed  PubMed Central  Google Scholar 

80.
Patel CN, Wortham BW, Lines JL, Fetherston JD, Perry RD, Oliveira MA. Polyamines are essential for the formation of plague biofilm. J Bacteriol. 2006;188:2355–63.
CAS  PubMed  PubMed Central  Google Scholar 

81.
Capdevila DA, Wang J, Giedroc DP. Bacterial strategies to maintain zinc metallostasis at the host–pathogen interface. J Biol Chem. 2016;291:20858–68.
CAS  PubMed  PubMed Central  Google Scholar 

82.
Schoepp-Cothenet B, van Lis R, Philippot P, Magalon A, Russell MJ, Nitschke W. The ineluctable requirement for the trans-iron elements molybdenum and/or tungsten in the origin of life. Sci Rep. 2012;2:263.
PubMed  PubMed Central  Google Scholar 

83.
Reda T, Plugge CM, Abram NJ, Hirst J. Reversible interconversion of carbon dioxide and formate by an electroactive enzyme. Proc Natl Acad Sci USA. 2008;105:10654–8.
CAS  PubMed  Google Scholar 

84.
Hartmann T, Schwanhold N, Leimkühler S. Assembly and catalysis of molybdenum or tungsten-containing formate dehydrogenases from bacteria. Biochim Biophys Acta. 2015;1854:1090–1100.
CAS  PubMed  Google Scholar 

85.
Ilbert M, Bonnefoy V. Insight into the evolution of the iron oxidation pathways. Biochim Biophys Acta. 2013;1827:161–75.
CAS  PubMed  Google Scholar 

86.
Lovley DR, Holmes DE, Nevin KP. Dissimilatory Fe(III) and Mn(IV) reduction. Adv Micro Physiol. 2004;49:219–86.
CAS  Google Scholar 

87.
Melton ED, Swanner ED, Behrens S, Schmidt C, Kappler A. The interplay of microbially mediated and abiotic reactions in the biogeochemical Fe cycle. Nat Rev Microbiol. 2014;12:797–808.
CAS  PubMed  Google Scholar 

88.
Maisch M, Lueder U, Laufer K, Scholze C, Kappler A, Schmidt C. Contribution of microaerophilic Iron(II)-oxidizers to Iron(III) mineral formation. Environ Sci Technol. 2019;53:8197–204.
CAS  PubMed  Google Scholar 

89.
Hong Y, Wu J, Wilson S, Song B. Vertical stratification of sediment microbial communities along geochemical gradients of a subterranean estuary located at the Gloucester Beach of Virginia, United States. Front Microbiol. 2018;9:3343.
PubMed  Google Scholar 

90.
Liptzin D, Silver WL. Spatial patterns in oxygen and redox sensitive biogeochemistry in tropical forest soils. Ecosphere. 2015;6:art211.
Google Scholar 

91.
Borer B, Tecon R, Or D. Spatial organization of bacterial populations in response to oxygen and carbon counter-gradients in pore networks. Nat Commun. 2018;9:769.
PubMed  PubMed Central  Google Scholar 

92.
Widder S, Allen RJ, Pfeiffer T, Curtis TP, Wiuf C, Sloan WT, et al. Challenges in microbial ecology: building predictive understanding of community function and dynamics. ISME J. 2016;10:2557–68.
PubMed  PubMed Central  Google Scholar 

93.
Frey PA, Reed GH. The ubiquity of iron. ACS Chem Biol. 2012;7:1477–81.
CAS  PubMed  Google Scholar 

94.
Edwards KJ, Bach W, McCollom TM, Rogers DR. Neutrophilic iron-oxidizing bacteria in the ocean: their habitats, diversity, and roles in mineral deposition, rock alteration, and biomass production in the deep-sea. Geomicrobiol J. 2004;21:393–404.
CAS  Google Scholar 

95.
Bondici VF, Khan NH, Swerhone GDW, Dynes JJ, Lawrence JR, Yergeau E, et al. Biogeochemical activity of microbial biofilms in the water column overlying uranium mine tailings. J Appl Microbiol. 2014;117:1079–94.
CAS  PubMed  Google Scholar 

96.
Lee AK, Newman DK. Microbial iron respiration: impacts on corrosion processes. Appl Microbiol Biotechnol. 2003;62:134–9.
CAS  PubMed  Google Scholar 

97.
Glasser NR, Saunders SH, Newman DK. The colorful world of extracellular electron shuttles. Annu Rev Microbiol. 2017;71:731–51.
CAS  PubMed  PubMed Central  Google Scholar 

98.
Philips J, Verbeeck K, Rabaey K, Arends JBA. Electron transfer mechanisms in biofilms. In: Scott K, Yu EH (eds). Microbial electrochemical and fuel cells. 2016. Woodhead Publishing, Sawston, Cambridge, United Kingdom, p. 67–113.

99.
Gao L, Lu X, Liu H, Li J, Li W, Song R, et al. Mediation of extracellular polymeric substances in microbial reduction of hematite by Shewanella oneidensis MR-1. Front Microbiol. 2019;10:575.
PubMed  PubMed Central  Google Scholar 

100.
Roden EE, McBeth JM, Blöthe M, Percak-Dennett EM, Fleming EJ, Holyoke RR, et al. The microbial ferrous wheel in a neutral pH groundwater seep. Front Microbiol. 2012;3:172.
PubMed  PubMed Central  Google Scholar  More

1.
Convention on Biological Diversity. Aichi biodiversity targets. Aichi Biodivers. Targets 9–10 https://www.cbd.int/sp/targets/ (2010).
2.
Gray, C. L. et al. Local biodiversity is higher inside than outside terrestrial protected areas worldwide. Nat. Commun. 7, 1–7 (2016).
Google Scholar 

3.
Joppa, L. N. & Pfaff, A. Global protected area impacts. Proc. R. Soc. B Biol. Sci. 278, 1633–1638 (2011).
Article  Google Scholar 

4.
Geldmann, J. et al. Effectiveness of terrestrial protected areas in reducing habitat loss and population declines. Biol. Conserv. 161, 230–238 (2013).
Article  Google Scholar 

5.
Coetzee, B. W. T., Gaston, K. J. & Chown, S. L. Local scale comparisons of biodiversity as a test for global protected area ecological performance: a meta-analysis. PLoS One 9, e105824 (2014).
ADS  Article  Google Scholar 

6.
UNEP-WCMC, IUCN & NGS. Protected Planet Live Report 2020. https://livereport.protectedplanet.net/ (2020).

7.
Visconti, B. P. et al. Protected area targets post-2020. Science 364, 239–241 (2019).
ADS  CAS  PubMed  Google Scholar 

8.
Jenkins, C. N., Van Houtan, K. S., Pimm, S. L. & Sexton, J. O. US protected lands mismatch biodiversity priorities. Proc. Natl. Acad. Sci. 112, 5081–5086 (2015).
ADS  CAS  Article  Google Scholar 

9.
Venter, O. et al. Bias in protected-area location and its effects on long-term aspirations of biodiversity conventions. Conserv. Biol. 32, 127–134 (2018).
Article  Google Scholar 

10.
USGS. U.S. Geological Survey Gap Analysis Project (GAP): Protected Areas Database of the United States (PAD-US). https://www.usgs.gov/core-science-systems/science-analytics-and-synthesis/gap/data-tools (2018).

11.
Comay, L. B., Crafton, R. E., Vincent, C. H. & Hoover, K. Federal Land Designations : A Brief Guide. https://fas.org/sgp/crs/misc/R45340.pdf (2018).

12.
Horton, G. Downsizing national monuments: The current debate and lessons from history. UCLA J. Environ. Law Policy 38, 79–102 (2020).
Google Scholar 

13.
Kamal, S., Grodzińska-Jurczak, M. & Brown, G. Conservation on private land: a review of global strategies with a proposed classification system. J. Environ. Plan. Manag. 58, 576–597 (2015).
Article  Google Scholar 

14.
Bargelt, L., Fortin, M. J. & Murray, D. L. Assessing connectivity and the contribution of private lands to protected area networks in the United States. PLoS ONE 15, 1–13 (2020).
Article  Google Scholar 

15.
Vergílio, M. et al. Assessing the efficiency of protected areas to represent biodiversity: A small island case study. Environ. Conserv. 43, 337–349 (2016).
Article  Google Scholar 

16.
Epperly, J. et al. Relationships between borders, management agencies, and the likelihood of watershed impairment. PLoS ONE 13, 1–14 (2018).
Article  Google Scholar 

17.
Betts, M. G. & Villard, M.-A. Landscape thresholds in species occurrence as quantitative targets in forest management: generality in space and time? Setting conservation targets for managed forest landscapes (ed. Villard & Jonsson) 185–206 (Cambridge University Press, 2009). doi:10.1017/cbo9781139175388.010

18.
Smith, J. R. et al. A global test of ecoregions. Nat. Ecol. Evol. 2, 1889–1896 (2018).
Article  Google Scholar 

19.
Small, C. & Nicholls, R. J. A global analysis of human settlement in coastal zones. J. Coast. Res. 19, 584–599 (2003).
Google Scholar 

20.
Le Saout, S. et al. Protected areas and effective biodiversity conservation. Science 342, 803–805 (2013).
ADS  Article  Google Scholar 

21.
Watson, J. E. M., Dudley, N., Segan, D. B. & Hockings, M. The performance and potential of protected areas. Nature 515, 67–73 (2014).
ADS  CAS  Article  Google Scholar 

22.
Deguise, I. & Kerr, J. Protected areas and prospects for endangered species conservation in Canada. Conserv. Biol. 20, 48–55 (2006).
Article  Google Scholar 

23.
Venter, O. et al. Targeting global protected area expansion for imperiled biodiversity. PLoS Biol. 12, https://doi.org/10.1371/journal.pbio.1001891 (2014).

24.
Mittermeier, R. A. et al. Wilderness and biodiversity conservation. Proc. Natl. Acad. Sci. 100, 10309–10313 (2003).
ADS  CAS  Article  Google Scholar 

25.
Kukkonen, M. O. & Tammi, I. Systematic reassessment of Laos’ protected area network. Biol. Conserv. 229, 142–151 (2019).
Article  Google Scholar 

26.
Prieto-Torres, D. A., Nori, J. & Rojas-Soto, O. R. Identifying priority conservation areas for birds associated to endangered Neotropical dry forests. Biol. Conserv. 228, 205–214 (2018).
Article  Google Scholar 

27.
Jones, K. R. et al. One-third of global protected land is under intense human pressure. Science 360, 788–791 (2018).
CAS  Article  Google Scholar 

28.
MRLC. 2001 National land cover database. https://www.mrlc.gov/ (2005).

29.
Adams, V. M., Pressey, R. L. & Naidoo, R. Opportunity costs: who really pays for conservation?. Biol. Conserv. 143, 439–448 (2010).
Article  Google Scholar 

30.
Sutton, N. J., Cho, S. & Armsworth, P. R. A reliance on agricultural land values in conservation planning alters the spatial distribution of priorities and overestimates the acquisition costs of protected areas. Biol. Conserv. 194, 2–10 (2016).
Article  Google Scholar 

31.
Merenlender, A. M., Huntsinger, L., Guthey, G. & Fairfax, S. K. Land trusts and conservation easements: who is conserving what for whom?. Conserv. Biol. 18, 65–75 (2004).
Article  Google Scholar 

32.
Cortés Capano, G., Toivonen, T., Soutullo, A. & Di Minin, E. The emergence of private land conservation in scientific literature: a review. Biol. Conserv. 237, 191–199 (2019).
Article  Google Scholar 

33.
Hooper, D. U. et al. A global synthesis reveals biodiversity loss as a major driver of ecosystem change. Nature 486, 105–108 (2012).
ADS  CAS  Article  Google Scholar 

34.
The Nature Conservancy. TNC terrestrial Ecoregions. (2009).

35.
Omernik, J. M. & Griffith, G. E. Ecoregions of the conterminous United States: evolution of a hierarchical spatial framework. Environ. Manage. 54, 1249–1266 (2014).
ADS  Article  Google Scholar 

36.
USGS Gap Analysis Program. Protected Areas Database of the United States (PAD-US), version 1.4 [vector digital data]. https://www.sciencebase.gov/catalog/item/5963ea3fe4b0d1f9f059d955 (2016).

37.
Baldwin, R. F. & Fouch, N. T. Understanding the biodiversity contributions of small protected areas presents many challenges. Land https://doi.org/10.3390/land7040123 (2018).
Article  Google Scholar 

38.
Luja, V. H., Navarro, C. J., Torres Covarrubias, L. A., Cortés Hernández, M. & Vallarta Chan, I. L. Small protected areas as stepping-stones for jaguars in western Mexico. Trop. Conserv. Sci. 10, 194008291771705 (2017).
Article  Google Scholar 

39.
Saura, S., Bodin, Ö & Fortin, M. J. Stepping stones are crucial for species’ long-distance dispersal and range expansion through habitat networks. J. Appl. Ecol. 51, 171–182 (2014).
Article  Google Scholar 

40.
Pebesma, E., Bivand, R., Rowlingson, B. & Gomez-Rubio, V. Sp: classes and methods for spatial data. http//CRAN.R-project.org/package=sp, R Packag. version 1.0–14 (2013).

41.
Hijmans, R. J. et al. Raster: raster: Geographic data analysis and modeling. R Packag. version 2–0 (2011).

42.
Nicholas J. Lewin-Koh contributions by Edzer J. Pebesma, Eric Archer, Adrian Baddeley, Hans-Jörg Bibiko, Stéphane Dray, David Forrest, Patrick Giraudoux, Duncan Golicher, Virgilio Gómez Rubio, Patrick Hausmann, Thomas Jagger, Sebastian P. Luque, Don MacQ, R. B. maptools: Tools for reading and handling spatial objects. (2009).

43.
Bivand, R., Keitt, T. & Rowlingson, B. rgdal: Bindings for the geospacial data abstraction library. (2013).

44.
Bivand, R., Rundel, C., Pebesma, E. & Hufthammer, K. O. Interface to geometry engine – open source (GEOS): Package ‘rgeos’. R Documentation (2016).

45.
Tennekes, M. et al. tmap: Thematic maps. (2019).

46.
R Development Core Team. R: A language and environment for statistical computing. https://www.R-project.org. [Google Scholar] (2019).

47.
US Fish and Wildlife Service. Environmental conservation online system. USFWS, https://ecos.fws.gov/ecp/. (2016).

48.
Ricketts, T. & Imhoff, M. Biodiversity, urban areas, and agriculture: Locating priority ecoregions for conservation. Ecol. Soc. 8, https://www.ecologyandsociety.org/vol8/iss2/art1/ (2003).

49.
Lamoreux, J. F. et al. Global tests of biodiversity concordance and the importance of endemism. Nature 440, 212–214 (2006).
ADS  CAS  Article  Google Scholar 

50.
US Endowment for Forestry and Communities. National conservation easement database. https://www.conservationeasement.us/ (2014).

51.
Bureau of Land Management. BLM National Surface Management Agency GIS. (2019). More

Field experiment
Study design
In 2017, eight unmanaged meadows were selected in the Prealps of Switzerland. This region has low levels of light emission with a radiance lower than 0.25 × 10-9 W sr-1 cm-2 (data from https://www.lightpollutionmap.info). Meadows had an average linear distance to the nearest site of 1.45 ± 0.34 km. The sites were located in the middle of the meadows on as homogenous vegetation as possible, so that there was no influence by elements like bushes or forest edges. The most abundant and widespread plant species on the meadows was Cirsium oleraceum (Asteraceae), followed by other plant species being abundant but not present on all sampling sites: Angelica sylvestris (Apiaceae), Eupatorium cannabinum (Asteraceae), Erigeron annuus s.l. (Asteraceae) and Filipendula ulmaria (Rosaceae). On four out of the eight meadows we experimentally installed a LED street lamp (Schréder GmbH, type: AMPERA MIDI 48 LED, colour temperature: neutral white (4,000 K), nominal LED flux: 6,800 lm) on 6 m high poles. Street lamps were installed on one side of the meadows, which resulted in an experimental set-up, where during nighttime a part of the meadow was illuminated by a cone of light. The part of the meadow further from the experimentally set-up street lamp was not illuminated and its darkness corresponded to the darkness measured on the control meadows that had no artificial light source in the vicinity. In other words, the four meadows were divided by artificial light into two parts, one directly illuminated by the lamp and the other being dark but adjacent to the illuminated part. Subsequently, we refer to the two parts as two sites, even though they were part of the same meadow, i.e., the illuminated part is further referred to as illuminated site, the dark part adjacent to the illuminated part as adjacent site (see Fig. 1). It is important to notice, that the street lamp was experimentally established, i.e., there was no systematic bias in terms of other landscape structures (such as roads, forest edges or hedges) where the illuminated part of the meadow was, adjacent, respectively. Thus, landscape structures that were different between the illuminated and dark part of a meadow potentially influenced the results in a non-systematic way and increased variance, but did not create a systematic bias. The remaining four meadows were left completely dark (further referred to as dark control sites), but they were equipped with a fake street lamp to provide comparable conditions. Light intensity on illuminated sites followed a negative exponential curve as function of the distance from the lamp dropping from 75.73 ± 1.54 lx just under the lamp ( More

1.
World Health Organization. Coronavirus disease (COVID-19) advice for the public: Myth busters 2020 [cited 2020 2020/05/22]. Available from: https://www.who.int/emergencies/diseases/novel-coronavirus-2019/advice-for-public/myth-busters.
2.
Chandrashekar, A., Liu, J., Martinot, A. J., McMahan, K., Mercado, N, B,, Peter, L. et al. SARS-CoV-2 infection protects against rechallenge in rhesus macaques. Science (2020).

3.
Huang, C. et al. Clinical features of patients infected with 2019 novel coronavirus in Wuhan, China. Lancet 395(10223), 497–506 (2020).
CAS  PubMed  PubMed Central  Article  Google Scholar 

4.
Turell, M. J., Dohm, D. J., Geden, C. J., Hogsette, J. A. & Linthicum, K. J. Potential for stable flies and house flies (Diptera: Muscidae) to transmit Rift Valley fever virus. J. Am. Mosq. Control Assoc. 26(4), 445–448 (2010).
PubMed  Article  Google Scholar 

5.
Higgs, S., Schneider, B. S., Vanlandingham, D. L., Klingler, K. A. & Gould, E. A. Nonviremic transmission of West Nile virus. Proc. Natl. Acad. Sci. USA. 102(25), 8871–8874 (2005).
ADS  CAS  PubMed  Article  Google Scholar 

6.
McGee, C. E., Schneider, B. S., Girard, Y. A., Vanlandingham, D. L. & Higgs, S. Nonviremic transmission of West Nile virus: evaluation of the effects of space, time, and mosquito species. Am. J. Trop. Med .Hyg. 76(3), 424–430 (2007).
PubMed  Article  Google Scholar 

7.
Reisen, W. K., Fang, Y. & Martinez, V. Is nonviremic transmission of West Nile virus by Culex mosquitoes (Diptera: Culicidae) nonviremic?. J. Med. Entomol. 44(2), 299–302 (2007).
PubMed  Article  Google Scholar 

8.
Rosen, L. The use of Toxorhynchites mosquitoes to detect and propagate dengue and other arboviruses. Am. J. Trop. Med. Hyg. 30(1), 177–183 (1981).
CAS  PubMed  Article  Google Scholar 

9.
Rosen, L. & Gubler, D. The use of mosquitoes to detect and propagate dengue viruses. Am. J. Trop. Med. Hyg. 23(6), 1153–1160 (1974).
CAS  PubMed  Article  Google Scholar 

10.
Peloquin, J. J., Thomas, T. A. & Higgs, S. Pink bollworm larvae infection with a double subgenomic Sindbis (dsSIN) virus to express genes of interest. J. Cotton Sci. 5(2), 114–120 (2001).
CAS  Google Scholar 

11.
Lewis, D. L. et al. Ectopic gene expression and homeotic transformations in arthropods using recombinant Sindbis viruses. Curr. Biol. 9(22), 1279–1287 (1999).
CAS  PubMed  Article  Google Scholar 

12.
Vaughan, J. A., Trpis, M. & Turell, M. J. Brugia malayi microfilariae (Nematoda: Filaridae) enhance the infectivity of Venezuelan equine encephalitis virus to Aedes mosquitoes (Diptera: Culicidae). J. Med. Entomol. 36(6), 758–763 (1999).
CAS  PubMed  Article  Google Scholar 

13.
Centers for Disease Control and Prevention. International Catalog of Arboviruses. In: Prevention CfDCa, editor. Atlanta, GA: Center for Disease Control and Prevention; 1985.

14.
Traavik, T., Mehl, R. & Kjeldsberg, E. “Runde” virus, a coronavirus-like agent associated with seabirds and ticks. Arch. Virol. 55(1–2), 25–38 (1977).
CAS  PubMed  PubMed Central  Article  Google Scholar 

15.
Calibeo-Hayes, D. et al. Mechanical transmission of turkey coronavirus by domestic houseflies (Musca domestica Linnaeaus). Avian Dis. 47(1), 149–153 (2003).
PubMed  Article  Google Scholar 

16.
Fauver, J. R. et al. The use of xenosurveillance to detect human bacteria, parasites, and viruses in mosquito bloodmeals. Am. J. Trop. Med. Hyg. 97(2), 324–329 (2017).
CAS  PubMed  PubMed Central  Article  Google Scholar 

17.
Higgs, S. et al. Growth characteristics of ChimeriVax-Den vaccine viruses in Aedes aegypti and Aedes albopictus from Thailand. Am. J. Trop. Med. Hyg. 75(5), 986–993 (2006).
PubMed  Article  Google Scholar 

18.
Wendell, M. D., Wilson, T. G., Higgs, S. & Black, W. C. Chemical and gamma-ray mutagenesis of the white gene in Aedes aegypti. Insect Mol. Biol. 9(2), 119–125 (2000).
CAS  PubMed  Article  Google Scholar 

19.
Park, S. L., Huang, Y. S., Higgs, S. & Vanlandingham, D. L. Application of a nonpaper based matrix to preserve chikungunya virus infectivity at ambient temperature. Vector Borne Zoo. Dis. 18(5), 278–281 (2018).
Article  Google Scholar 

20.
Huang, Y. J. et al. Culex species mosquitoes and Zika virus. Vector Borne Zoo. Dis. 16(10), 673–676 (2016).
Article  Google Scholar 

21.
Huang, Y. S. et al. Differential outcomes of Zika virus infection in Aedes aegypti orally challenged with infectious blood meals and infectious protein meals. PLoS ONE 12(8), e0182386 (2017).
PubMed  PubMed Central  Article  Google Scholar 

22.
Ayers, V. B. et al. Culex tarsalis is a competent vector species for Cache Valley virus. Parasit. Vectors. 11(1), 519 (2018).
PubMed  PubMed Central  Article  Google Scholar 

23.
Ayers, V. B. et al. Infection and transmission of Cache Valley virus by Aedes albopictus and Aedes aegypti mosquitoes. Parasit. Vectors. 12(1), 384 (2019).
PubMed  PubMed Central  Article  Google Scholar 

24.
Tsetsarkin, K. A., Vanlandingham, D. L., McGee, C. E. & Higgs, S. A single mutation in chikungunya virus affects vector specificity and epidemic potential. PLoS Pathog. 3(12), e201 (2007).
PubMed  PubMed Central  Article  Google Scholar 

25.
Nuckols, J. T. et al. Evaluation of simultaneous transmission of chikungunya virus and dengue virus type 2 in infected Aedes aegypti and Aedes albopictus (Diptera: Culicidae). J. Med. Entomol. 52(3), 447–451 (2015).
CAS  PubMed  PubMed Central  Article  Google Scholar 

26.
Cook, C. L. et al. North American Culex pipiens and Culex quinquefasciatus are competent vectors for Usutu virus. PLoS Negl. Trop. Dis. 12(8), e0006732 (2018).
PubMed  PubMed Central  Article  Google Scholar  More

1.
Thompson LR, Sanders JG, McDonald D, Amir A, Ladau J, Locey KJ, et al. A communal catalogue reveals Earth’s multiscale microbial diversity. Nature. 2017;551:457–63.
CAS  PubMed  PubMed Central  Google Scholar 
2.
Parfrey LW, Moreau CS, Russell JA. Introduction: the host-associated microbiome: pattern, process and function. Mol Ecol. 2018;27:1749–65.
PubMed  Google Scholar 

3.
Moran NA, Ochman H, Hammer TJ. Evolutionary and ecological consequences of gut microbial communities. Annu Rev Ecol Evol Syst. 2019;50:451–75.
Google Scholar 

4.
McFall-Ngai M, Hadfield MG, Bosch TCG, Carey HV, Domazet-Loso T, Douglas AE, et al. Animals in a bacterial world, a new imperative for the life sciences. Proc Natl Acad Sci USA. 2013;110:3229–36.
CAS  PubMed  PubMed Central  Google Scholar 

5.
Colston TJ, Jackson CR. Microbiome evolution along divergent branches of the vertebrate tree of life: what is known and unknown. Mol Ecol. 2016;25:3776–800.
PubMed  Google Scholar 

6.
O’Hara AM, Shanahan F. The gut flora as a forgotten organ. EMBO Rep. 2006;7:688–93.
PubMed  PubMed Central  Google Scholar 

7.
Browne HP, Neville BA, Forster SC, Lawley TD. Transmission of the gut microbiota: spreading of health. Nat Rev Microbiol. 2017;15:531–43.
PubMed  PubMed Central  Google Scholar 

8.
Mao K, Baptista AP, Tamoutounour S, Zhuang L, Bouladoux N, Martins AJ, et al. Innate and adaptive lymphocytes sequentially shape the gut microbiota and lipid metabolism. Nature. 2018;554:255–9.
CAS  PubMed  Google Scholar 

9.
Belkaid Y, Hand TW. Role of the microbiota in immunity and inflammation. Cell. 2014;157:121–41.
CAS  PubMed  PubMed Central  Google Scholar 

10.
Sherwin E, Bordenstein SR, Quinn JL, Dinan TG, Cryan JF. Microbiota and the social brain. Science. 2019;366:eaar2016.
CAS  PubMed  Google Scholar 

11.
Buffie CG, Pamer EG. Microbiota-mediated colonization resistance against intestinal pathogens. Nat Rev Immunol. 2013;13:790–801.
CAS  PubMed  PubMed Central  Google Scholar 

12.
Clemente JC, Ursell LK, Parfrey LW, Knight R. The impact of the gut microbiota on human health: an integrative view. Cell. 2012;148:1258–70.
CAS  PubMed  PubMed Central  Google Scholar 

13.
Rosenbaum M, Knight R, Leibel RL. The gut microbiota in human energy homeostasis and obesity. Trends Endocrinol Metab. 2015;26:493–501.
CAS  PubMed  PubMed Central  Google Scholar 

14.
Foster KR, Schluter J, Coyte KZ, Rakoff-Nahoum S. The evolution of the host microbiome as an ecosystem on a leash. Nature. 2017;548:43–51.
CAS  PubMed  PubMed Central  Google Scholar 

15.
Knowles SCL, Eccles RM, Baltrūnaitė L. Species identity dominates over environment in shaping the microbiota of small mammals. Ecol Lett. 2019;22:826–37.
CAS  PubMed  Google Scholar 

16.
Henderson G, Cox F, Ganesh S, Jonker A, Young W, Janssen PH, et al. Rumen microbial community composition varies with diet and host, but a core microbiome is found across a wide geographical range. Sci Rep. 2015;5:14567.
CAS  PubMed  PubMed Central  Google Scholar 

17.
Sonnenburg ED, Smits SA, Tikhonov M, Higginbottom SK, Wingreen NS, Sonnenburg JL. Diet-induced extinctions in the gut microbiota compound over generations. Nature. 2016;529:212–5.
CAS  PubMed  PubMed Central  Google Scholar 

18.
Carmody Rachel N, Gerber Georg K, Luevano Jesus M Jr., Gatti Daniel M, Somes L, Svenson Karen L, et al. Diet dominates host genotype in shaping the murine gut microbiota. Cell Host Microbe. 2015;17:72–84.
CAS  PubMed  Google Scholar 

19.
David LA, Maurice CF, Carmody RN, Gootenberg DB, Button JE, Wolfe BE, et al. Diet rapidly and reproducibly alters the human gut microbiome. Nature. 2014;505:559–63.
CAS  PubMed  Google Scholar 

20.
Seedorf H, Griffin Nicholas W, Ridaura Vanessa K, Reyes A, Cheng J, Rey Federico E, et al. Bacteria from diverse habitats colonize and compete in the mouse gut. Cell. 2014;159:253–66.
CAS  PubMed  PubMed Central  Google Scholar 

21.
Hildebrand F, Nguyen TLA, Brinkman B, Yunta RG, Cauwe B, Vandenabeele P, et al. Inflammation-associated enterotypes, host genotype, cage and inter-individual effects drive gut microbiota variation in common laboratory mice. Genome Biol. 2013;14:R4.
PubMed  PubMed Central  Google Scholar 

22.
Schloss PD, Iverson KD, Petrosino JF, Schloss SJ. The dynamics of a family’s gut microbiota reveal variations on a theme. Microbiome. 2014;2:25.
PubMed  PubMed Central  Google Scholar 

23.
Song SJ, Lauber C, Costello EK, Lozupone CA, Humphrey G, Berg-Lyons D, et al. Cohabiting family members share microbiota with one another and with their dogs. eLife. 2013;2:e00458.
PubMed  PubMed Central  Google Scholar 

24.
Maurice CF, Cl Knowles S, Ladau J, Pollard KS, Fenton A, Pedersen AB, et al. Marked seasonal variation in the wild mouse gut microbiota. ISME J. 2015;9:2423–34.
CAS  PubMed  PubMed Central  Google Scholar 

25.
Ren T, Boutin S, Humphries MM, Dantzer B, Gorrell JC, Coltman DW, et al. Seasonal, spatial, and maternal effects on gut microbiome in wild red squirrels. Microbiome. 2017;5:163.
PubMed  PubMed Central  Google Scholar 

26.
Wang J, Chen L, Zhao N, Xu X, Xu Y, Zhu B. Of genes and microbes: solving the intricacies in host genomes. Protein Cell. 2018;9:446–61.
PubMed  PubMed Central  Google Scholar 

27.
Rothschild D, Weissbrod O, Barkan E, Kurilshikov A, Korem T, Zeevi D, et al. Environment dominates over host genetics in shaping human gut microbiota. Nature. 2018;555:210–5.
CAS  PubMed  Google Scholar 

28.
Amato KR, G. Sanders J, Song SJ, Nute M, Metcalf JL, Thompson LR, et al. Evolutionary trends in host physiology outweigh dietary niche in structuring primate gut microbiomes. ISME J. 2019;13:576–87.
CAS  PubMed  Google Scholar 

29.
Nishida AH, Ochman H. Rates of gut microbiome divergence in mammals. Mol Ecol. 2018;27:1884–97.
PubMed  PubMed Central  Google Scholar 

30.
Brooks AW, Kohl KD, Brucker RM, van Opstal EJ, Bordenstein SR. Phylosymbiosis: relationships and functional effects of microbial communities across host evolutionary history. PLoS Biol. 2016;14:e2000225.
PubMed  PubMed Central  Google Scholar 

31.
Ochman H, Worobey M, Kuo C-H, Ndjango J-BN, Peeters M, Hahn BH, et al. Evolutionary relationships of wild hominids recapitulated by gut microbial communities. PLoS Biol. 2010;8:e1000546.
PubMed  PubMed Central  Google Scholar 

32.
Kartzinel TR, Hsing JC, Musili PM, Brown BRP, Pringle RM. Covariation of diet and gut microbiome in African megafauna. Proc Natl Acad Sci USA. 2019;116:23588–93.
CAS  PubMed  Google Scholar 

33.
Muegge BD, Kuczynski J, Knights D, Clemente JC, González A, Fontana L, et al. Diet drives convergence in gut microbiome functions across mammalian phylogeny and within humans. Science. 2011;332:970–4.
CAS  PubMed  PubMed Central  Google Scholar 

34.
Delsuc F, Metcalf JL, Wegener Parfrey L, Song SJ, González A, Knight R. Convergence of gut microbiomes in myrmecophagous mammals. Mol Ecol. 2014;23:1301–17.
CAS  PubMed  Google Scholar 

35.
Ley RE, Hamady M, Lozupone C, Turnbaugh PJ, Ramey RR, Bircher JS, et al. Evolution of mammals and their gut microbes. Science. 2008;320:1647–51.
CAS  PubMed  PubMed Central  Google Scholar 

36.
Ruiz-Rodríguez M, Martín-Vivaldi M, Martínez-Bueno M, Soler JJ. Gut microbiota of great spotted cuckoo nestlings is a mixture of those of their foster magpie siblings and of cuckoo adults. Genes. 2018;9:381.
PubMed Central  Google Scholar 

37.
Davies NB. Cuckoo adaptations: trickery and tuning. J Zool. 2011;284:1–14.
Google Scholar 

38.
Payne RB. The cuckoos. New York: Oxford University Press; 2005.
Google Scholar 

39.
Prum RO, Berv JS, Dornburg A, Field DJ, Townsend JP, Lemmon EM, et al. A comprehensive phylogeny of birds (Aves) using targeted next-generation DNA sequencing. Nature. 2015;526:569–73.
CAS  Google Scholar 

40.
Soler M, Martínez JG, Soler JJ, Møller AP. Preferential allocation of food by magpie Pica pica to great spotted cuckoo Clamator glandarius chicks. Behav Ecol Sociobiol. 1995;37:7–13.
Google Scholar 

41.
Soler JJ, Martínez JG, Soler M, Møller AP. Coevolutionary interactions in a host-parasite system. Ecol Lett. 2001;4:470–6.
Google Scholar 

42.
Birkhead TR. The Magpies. The ecology and behaviour of black-billed and yellow-billed magpies. London: T & A D Poyser; 1991.
Google Scholar 

43.
Ruiz-Rodríguez M, Lucas FS, Heeb P, Soler JJ. Differences in intestinal microbiota between avian brood parasites and their hosts. Biol J Linn Soc. 2009;96:406–14.
Google Scholar 

44.
Soler JJ, Martin-Galvez D, De Neve L, Soler M. Brood parasitism correlates with the strength of spatial autocorrelation of life history and defensive traits in Magpies. Ecology. 2013;94:1338–46.
PubMed  Google Scholar 

45.
Moreno-Rueda G, Soler M, Soler JJ, Martínez JG, Pérez-Contreras T. Rules of food allocation between nestlings of the black-billed magpie Pica pica, a species showing brood reduction. Ardeola. 2007;54:15–25.
Google Scholar 

46.
Soler M, Soler JJ, Martínez JG. Duration of sympatry and coevolution between the great spotted cuckoo (Clamator glandarius) and its primary host, the magpie (Pica pica). In: Rothstein SI, SK Robinson SK, editors. Parasitic Birds and their hosts, studies in coevolution. Oxford: Oxford University Press; 1998. p. 113–28.

47.
Soler M, Soler JJ. Growth and development of great spotted cuckoos and their magpie host. Condor. 1991;93:49–54.
Google Scholar 

48.
Martín-Gálvez D, Pérez-Contreras T, Soler M, Soler JJ. Benefits associated with escalated begging behaviour of black-billed magpie nestlings overcompensate the associated energetic costs. J Exp Biol. 2011;214:1463–72.
PubMed  Google Scholar 

49.
Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, et al. QIIME allows analysis of high-throughput community sequencing data. Nat Methods. 2010;7:335–6.
CAS  PubMed  PubMed Central  Google Scholar 

50.
Bolyen E, Rideout JR, Dillon MR, Bokulich NA, Abnet CC, Al-Ghalith GA, et al. Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nat Biotechnol. 2019;37:852–7.
CAS  PubMed  PubMed Central  Google Scholar 

51.
Amir A, McDonald D, Navas-Molina JA, Kopylova E, Morton JT, Zech Xu Z, et al. Deblur rapidly resolves single-nucleotide community sequence patterns. mSystems. 2017;2:e00191–00116.
PubMed  PubMed Central  Google Scholar 

52.
Janssen S, McDonald D, Gonzalez A, Navas-Molina JA, Jiang L, Xu ZZ, et al. Phylogenetic placement of exact amplicon sequences improves associations with clinical information. mSystems. 2018;3:e00021–00018.
CAS  PubMed  PubMed Central  Google Scholar 

53.
DeSantis TZ, Hugenholtz P, Larsen N, Rojas M, Brodie EL, Keller K, et al. Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl Environ Microbiol. 2006;72:5069–72.
CAS  PubMed  PubMed Central  Google Scholar 

54.
Salter SJ, Cox MJ, Turek EM, Calus ST, Cookson WO, Moffatt MF, et al. Reagent and laboratory contamination can critically impact sequence-based microbiome analyses. BMC Biol. 2014;12:87.
PubMed  PubMed Central  Google Scholar 

55.
de Goffau MC, Lager S, Salter SJ, Wagner J, Kronbichler A, Charnock-Jones DS, et al. Recognizing the reagent microbiome. Nat Microbiol. 2018;3:851–3.
PubMed  Google Scholar 

56.
Whittaker RH. Evolution and measurement of species diversity. Taxon. 1972;21:213–51.
Google Scholar 

57.
Shannon CE. A mathematical theory of communication. Bell Labs Tech J. 1948;27:379–423.
Google Scholar 

58.
Lozupone C, Knight R. UniFrac: a new phylogenetic method for comparing microbial communities. Appl Environ Microbiol. 2005;71:8228–35.
CAS  PubMed  PubMed Central  Google Scholar 

59.
Lozupone CA, Hamady M, Kelley ST, Knight R. Quantitative and qualitative β diversity measures lead to different insights into factors that structure microbial communities. Appl Environ Microbiol. 2007;73:1576–85.
CAS  PubMed  PubMed Central  Google Scholar 

60.
Goslee SC, Urban DL. The ecodist package for dissimilarity-based analysis of ecological data. J Stat Softw. 2007;22:i07.
Google Scholar 

61.
Moeller A, Suzuki T, Lin D, Lacey E, Wasser S, Nachman M. Dispersal limitation promotes the diversification of the mammalian gut microbiota. Proc Natl Acad Sci USA. 2017;114:13768–73.
CAS  PubMed  Google Scholar 

62.
Moeller AH, Caro-Quintero A, Mjungu D, Georgiev AV, Lonsdorf EV, Muller MN, et al. Cospeciation of gut microbiota with hominids. Science. 2016;353:380–2.
CAS  PubMed  PubMed Central  Google Scholar 

63.
Groussin M, Mazel F, Sanders JG, Smillie CS, Lavergne S, Thuiller W, et al. Unraveling the processes shaping mammalian gut microbiomes over evolutionary time. Nat Commun. 2017;8:14319.
CAS  PubMed  PubMed Central  Google Scholar 

64.
Soler M, Soler JJ. Innate versus learned recognition of conspecifics in great spotted cuckoos Clamator glandarius. Anim Cogn. 1999;2:97–102.
Google Scholar 

65.
Donaldson GP, Ladinsky MS, Yu KB, Sanders JG, Yoo BB, Chou WC, et al. Gut microbiota utilize immunoglobulin A for mucosal colonization. Science. 2018;360:795–800.
CAS  PubMed  PubMed Central  Google Scholar 

66.
Thaiss CA, Zmora N, Levy M, Elinav E. The microbiome and innate immunity. Nature. 2016;535:65–74.
CAS  PubMed  Google Scholar 

67.
Sicard J-F, Le Bihan G, Vogeleer P, Jacques M, Harel J. Interactions of intestinal bacteria with components of the intestinal mucus. Front Cell Infect Microbiol. 2017;7:387.
PubMed  PubMed Central  Google Scholar 

68.
Soler JJ, Møller AP, Soler M, Martíne1z JG. Interactions between a brood parasite and its host in relation to parasitism and immune defence. Evol Ecol Res. 1999;1:189–210.
Google Scholar 

69.
Ruiz-Rodríguez M, Soler JJ, Lucas FS, Heeb P, Palacios M, Martín-Gálvez D, et al. Bacterial diversity at the cloaca relates to an immune response in magpie Pica pica and to body condition of great spotted cuckoo Clamator glandarius nestlings. J Avian Biol. 2009;40:42–8.
Google Scholar 

70.
Soler JJ, De Neve L, Pérez-Contreras T, Soler M, Sorci G. Trade-off between immunocompetence and growth in magpies: an experimental study. Proc R Soc Lond B Biol Sci. 2003;270:241–8.
Google Scholar 

71.
Soler M, Rubio LA, Perez-Contreras T, Ontanilla J, De Neve L. Intestinal digestibility of great spotted cuckoo nestlings is less efficient than that of magpie host nestlings. Biol J Linn Soc. 2017;122:675–80.
Google Scholar 

72.
Clayton JB, Vangay P, Huang H, Ward T, Hillmann BM, Al-Ghalith GA, et al. Captivity humanizes the primate microbiome. Proc Natl Acad Sci USA. 2016;113:10376–81.
CAS  PubMed  Google Scholar 

73.
Kohl K, Skopec M, Dearing MD. Captivity results in disparate loss of gut microbial diversity in closely related hosts. Cons Physiol. 2014;2:cou009.
Google Scholar  More