More stories

  • in

    Extreme temperatures compromise male and female fertility in a large desert bird

    1.
    Angilletta, M. J. Thermal Adaptation: A Theoretical And Empirical Analysis (Oxford University Press, 2009).
    2.
    Chown, S. L., Sinclair, B. J., Leinaas, H. P. & Gaston, K. J. Hemispheric asymmetries in biodiversity—a serious matter for ecology. PLoS Biol. 2, e406 (2004).
    PubMed  PubMed Central  Article  CAS  Google Scholar 

    3.
    Sunday, J. M., Bates, A. E. & Dulvy, N. K. Thermal tolerance and the global redistribution of animals. Nat. Clim. Change 2, 686–690 (2012).
    ADS  Article  Google Scholar 

    4.
    Kellermann, V., van Heerwaarden, B., Sgrò, C. M. & Hoffmann, A. A. Fundamental evolutionary limits in ecological traits drive Drosophila species distributions. Science 325, 1244–1246 (2009).
    ADS  CAS  PubMed  Article  Google Scholar 

    5.
    Araújo, M. B. et al. Heat freezes niche evolution. Ecol. Lett. 16, 1206–1219 (2013).
    PubMed  Article  Google Scholar 

    6.
    García-Robledo, C., Kuprewicz, E. K., Staines, C. L., Erwin, T. L. & Kress, W. J. Limited tolerance by insects to high temperatures across tropical elevational gradients and the implications of global warming for extinction. Proc. Natl Acad. Sci. USA 113, 680–685 (2016).
    ADS  PubMed  Article  CAS  Google Scholar 

    7.
    Geerts, A. N. et al. Rapid evolution of thermal tolerance in the water flea, Daphnia. Nat. Clim. Change 5, 665–668 (2015).
    ADS  Article  Google Scholar 

    8.
    Iossa, G. Sex-specific differences in thermal fertility limits. Trends Ecol. Evol. 34, 490–492 (2019).
    PubMed  Article  Google Scholar 

    9.
    Walsh, B. S. et al. The impact of climate change on fertility. Trends Ecol. Evol. 34, 249–259 (2019).
    PubMed  Article  Google Scholar 

    10.
    Vasudeva, R. et al. Adaptive thermal plasticity enhances sperm and egg performance in a model insect. eLife 8, e49452 (2019).
    PubMed  PubMed Central  Article  Google Scholar 

    11.
    Hurley, L. L., McDiarmid, C. S., Friesen, C. R., Griffith, S. C. & Rowe, M. Experimental heatwaves negatively impact sperm quality in the zebra finch. Proc. R. Soc. B 285, 20172547 (2018).
    PubMed  Article  Google Scholar 

    12.
    Dahlke, F., Wohlrab, S., Butzin, M. & Pörtner, H. Thermal bottlenecks in the lifecycle define climate vulnerability of fish. Science 369, 65–70 (2020).
    ADS  CAS  PubMed  PubMed Central  Article  Google Scholar 

    13.
    Bathiany, S., Dakos, V., Scheffer, M. & Lenton, T. M. Climate models predict increasing temperature variability in poor countries. Sci. Adv. 4, 1–11 (2018).
    Article  Google Scholar 

    14.
    Vázquez, D. P., Gianoli, E., Morris, W. F. & Bozinovic, F. Ecological and evolutionary impacts of changing climatic variability. Biol. Rev. 92, 22–42 (2017).
    PubMed  Article  Google Scholar 

    15.
    Chevin, L.-M., Lande, R. & Mace, G. M. Adaptation, plasticity, and extinction in a changing environment: towards a predictive theory. PLoS Biol. 8, e1000357 (2010).
    PubMed  PubMed Central  Article  CAS  Google Scholar 

    16.
    Sgrò, C. M. & Hoffmann, A. A. Genetic correlations, tradeoffs and environmental variation. Heredity 93, 241–248 (2004).
    PubMed  Article  Google Scholar 

    17.
    Wood, C. W. & Brodie, E. D. Environmental effects on the structure of the G-matrix. Evolution 69, 2927–2940 (2015).
    PubMed  Article  Google Scholar 

    18.
    Brommer, J. E., Merila, J., Sheldon, B. C. & Gustavsson, L. Natural selection and genetic variation for reproductive reaction norms in a wild bird population. Evolution 59, 1362–1371 (2005).
    PubMed  Article  Google Scholar 

    19.
    Brommer, J. E., Rattiste, K. & Wilson, A. J. Exploring plasticity in the wild: laying date–temperature reaction norms in the common gull Larus canus. Proc. R. Soc. B 275, 687–693 (2008).
    PubMed  Article  Google Scholar 

    20.
    Nussey, D. H., Postma, E., Gienapp, P., Visser, M. E. & Gienapp, P. Selection on heritable phenotypic plasticity in a wild bird population. Science 310, 304–306 (2005).
    ADS  CAS  PubMed  Article  Google Scholar 

    21.
    Charmantier, A. et al. Adaptive phenotypic plasticity in response to climate change in a wild bird population. Science 320, 800–803 (2008).
    ADS  CAS  PubMed  Article  Google Scholar 

    22.
    Matthysen, E., Adriaensen, F. & Dhondt, A. A. Multiple responses to increasing spring temperatures in the breeding cycle of blue and great tits (Cyanistes caeruleus, Parus major). Glob. Change Biol. 17, 1–16 (2011).
    ADS  Article  Google Scholar 

    23.
    Both, C. & Visser, M. E. Adjustment to climate change is constrained by arrival date in a long-distance migrant bird. Nature 411, 296–298 (2001).
    ADS  CAS  PubMed  Article  Google Scholar 

    24.
    Schiegg, K., Pasinelli, G., Walters, J. R. & Daniels, S. J. Inbreeding and experience affect response to climate change by endangered woodpeckers. Proc. R. Soc. B 269, 1153–1159 (2002).
    PubMed  Article  Google Scholar 

    25.
    Wilson, S., Norris, D. R., Wilson, A. G. & Arcese, P. Breeding experience and population density affect the ability of a songbird to respond to future climate variation. Proc. R. Soc. B 274, 2539–2545 (2007).
    PubMed  Article  Google Scholar 

    26.
    Dunn, P. O. & Winkler, D. W. Climate change has affected the breeding date of tree swallows throughout North America. Proc. R. Soc. B 266, 2487–2490 (1999).
    CAS  Article  Google Scholar 

    27.
    Hällfors, M. H. et al. Shifts in timing and duration of breeding for 73 boreal bird species over four decades. Proc. Natl Acad. Sci. USA 117, 18557–18565 (2020).
    PubMed  Article  CAS  Google Scholar 

    28.
    Gienapp, P., Postma, E. & Visser, M. E. Why breeding time has not responded to selection for earlier breeding in a songbird population. Evolution 60, 2381 (2006).
    PubMed  Article  Google Scholar 

    29.
    Jàrvinen, A. Global warming and egg size of birds. Ecography 17, 108–110 (1994).
    Article  Google Scholar 

    30.
    Kitaysky, A. S. & Golubova, E. G. Climate change causes contrasting trends in reproductive performance of planktivorous and piscivorous alcids. J. Anim. Ecol. 69, 248–262 (2000).
    Article  Google Scholar 

    31.
    Julliard, R., Clavel, J., Devictor, V., Jiguet, F. & Couvet, D. Spatial segregation of specialists and generalists in bird communities. Ecol. Lett. 9, 1237–1244 (2006).
    PubMed  Article  Google Scholar 

    32.
    Weatherhead, P. J. Effects of climate variation on timing of nesting, reproductive success, and offspring sex ratios of red-winged blackbirds. Oecologia 144, 168–175 (2005).
    ADS  PubMed  Article  Google Scholar 

    33.
    Auer, S. K. & Martin, T. E. Climate change has indirect effects on resource use and overlap among coexisting bird species with negative consequences for their reproductive success. Glob. Change Biol. 19, 411–419 (2013).
    ADS  Article  Google Scholar 

    34.
    Riddell, E. A., Iknayan, K. J., Wolf, B. O., Sinervo, B. & Beissinger, S. R. Cooling requirements fueled the collapse of a desert bird community from climate change. Proc. Natl Acad. Sci. USA116, 21609–21615 (2019).
    CAS  PubMed  Article  Google Scholar 

    35.
    Visser, M. E., Van Noordwijk, A. J., Tinbergen, J. M. & Lessells, C. M. Warmer springs lead to mistimed reproduction in great tits (Parus major). Proc. R. Soc. B 265, 1867–1870 (1998).
    Article  Google Scholar 

    36.
    Both, C., Bouwhuis, S., Lessells, C. M. & Visser, M. E. Climate change and population declines in a long-distance migratory bird. Nature 441, 81–83 (2006).
    ADS  CAS  PubMed  Article  Google Scholar 

    37.
    Magige, F. J., Stokke, B. G., Sortland, R. & Røskaft, E. Breeding biology of ostriches (Struthio camelus) in the Serengeti ecosystem, Tanzania. Afr. J. Ecol. 47, 400–408 (2009).
    Article  Google Scholar 

    38.
    Bertram, B. C. R. The Ostrich Communal Nesting System (Princeton University Press, New Jersey, 1992).

    39.
    Kimwele, C. N. & Graves, J. A. A molecular genetic analysis of the communal nesting of the ostrich (Struthio camelus). Mol. Ecol. 12, 229–236 (2003).
    CAS  PubMed  Article  Google Scholar 

    40.
    Maloney, S. K. Thermoregulation in ratites: a review. Aust. J. Exp. Agric. 48, 1293–1301 (2008).
    Article  Google Scholar 

    41.
    Hassan, S. M., Siam, A. A., Mady, M. E. & Cartwright, A. L. Egg storage period and weight effects on hatchability of ostrich (Struthio camelus) eggs. Poult. Sci. 84, 1908–1912 (2005).
    CAS  PubMed  Article  Google Scholar 

    42.
    Gonzalez, A., Satterlee, D. G., Moharer, F. & Cadd, G. G. Factors affecting ostrich egg hatchability. Poult. Sci. 78, 1257–1262 (1999).
    CAS  PubMed  Article  Google Scholar 

    43.
    Roff, D. A. & Wilson, A. J. Quantifying genotype-by-environment interactions in laboratory systems. In Genotype‐by‐Environment Interactions and Sexual Selection (eds. Hunt, J. & Hosken, D.) 100–136 (John Wiley & Sons, Ltd, 2014).

    44.
    Christians, J. K. Avian egg size: variation within species and inflexibility within individuals. Biol. Rev. Camb. Philos. Soc. 77, 1–26 (2002).
    PubMed  Article  Google Scholar 

    45.
    Lack, D. The Natural Regulation of Animal Numbers (Clarendon Press, 1954).

    46.
    Perrins, C. M. The timing of birds‘ breeding seasons. Ibis 112, 242–255 (1970).
    Article  Google Scholar 

    47.
    Sales, K. et al. Experimental heatwaves compromise sperm function and cause transgenerational damage in a model insect. Nat. Commun. 9, 1–11 (2018).
    ADS  CAS  Article  Google Scholar 

    48.
    McAfee, A. et al. Vulnerability of honey bee queens to heat-induced loss of fertility. Nat. Sustain 3, 367–376 (2020).
    Article  Google Scholar 

    49.
    Pérez-Crespo, M., Pintado, B. & Gutiérrez-Adán, A. Scrotal heat stress effects on sperm viability, sperm DNA integrity, and the offspring sex ratio in mice. Mol. Reprod. Dev. 75, 40–47 (2008).
    PubMed  Article  CAS  Google Scholar 

    50.
    Hansen, P. J. Effects of heat stress on mammalian reproduction. Philos. Trans. R. Soc. B 364, 3341–3350 (2009).
    Article  Google Scholar 

    51.
    Moreno, R. D., Lagos-Cabre, R., Bunay, J., Urzua, N. & Bustamante-Marin, X. Molecular basis of heat stress damage in mammalian testis. In Testis: Anatomy, Physiology and Pathology (eds. Nemoto, Y. & Inaba, N.) 127–155 (Nova Science, 2012).

    52.
    Karaca, A. G., Parker, H. M., Yeatman, J. B. & McDaniel, C. D. The effects of heat stress and sperm quality classification on broiler breeder male fertility and semen ion concentrations. Br. Poult. Sci. 43, 621–628 (2002).
    CAS  PubMed  Article  Google Scholar 

    53.
    Mita, P., Hinton, B. T. & Dufour, J. M. The blood–testis and blood–epididymis barriers are more than just their tight junctions. Biol. Reprod. 84, 851–858 (2011).
    Article  CAS  Google Scholar 

    54.
    Smith, C. C. & Fretwell, S. D. The optimal balance between size and number of offspring. Am. Nat. 108, 499–506 (1974).
    Article  Google Scholar 

    55.
    Ojanen, M. Composition of the eggs of the great tit (Parus major) and pied flycatcher (Ficedula hypoleuca). Ann. Zool. Fenn. 20, 57–63 (1983).
    Google Scholar 

    56.
    Krist, M. Egg size and offspring quality: a meta-analysis in birds. Biol. Rev. 86, 692–716 (2011).
    PubMed  Article  Google Scholar 

    57.
    Falconer, D. S. & Mackay, T. F. C. Introduction to Quantitative Genetics (Pearson, 1996).

    58.
    Lynch, M. & Gabriel, W. Environmental tolerance. Am. Nat. 129, 283–303 (1987).
    Article  Google Scholar 

    59.
    Gilchrist, G. W. Specialists and generalists in changing environments. I. Fitness landscapes of thermal sensitivity. Am. Nat. 146, 252–270 (1995).
    Article  Google Scholar 

    60.
    Whitlock, M. C. The red queen beats the jack-of-all-trades: the limitations on the evolution of phenotypic plasticity and niche breadth. Am. Nat. 148, S65 (1996).
    Article  Google Scholar 

    61.
    Pen, I. & Weissing, F. J. Towards a unified theory of cooperative breeding: the role of ecology and life history re-examined. Proc. R. Soc. B 267, 2411–2418 (2000).
    Article  Google Scholar 

    62.
    Emlen, S. T. The evolution of helping. I. An ecological constraints model. Am. Nat. 119, 29–39 (1982).
    Article  Google Scholar 

    63.
    Rubenstein, D. R. Spatiotemporal environmental variation, risk aversion, and the evolution of cooperative breeding as a bet-hedging strategy. Proc. Natl Acad. Sci. USA 108, 10816–10822 (2011).
    ADS  CAS  PubMed  Article  Google Scholar 

    64.
    Cornwallis, C. K. et al. Cooperation facilitates the colonization of harsh environments. Nat. Ecol. Evol. 1, 0057 (2017).
    Article  Google Scholar 

    65.
    Rubenstein, D. R. & Lovette, I. J. Temporal environmental variability drives the evolution of cooperative breeding in birds. Curr. Biol. 17, 1414–1419 (2007).
    CAS  PubMed  Article  Google Scholar 

    66.
    Albright, T. P. et al. Mapping evaporative water loss in desert passerines reveals an expanding threat of lethal dehydration. Proc. Natl Acad. Sci. USA 114, 201613625 (2017).
    Google Scholar 

    67.
    Vincze, O. et al. Parental cooperation in a changing climate: fluctuating environments predict shifts in care division. Glob. Ecol. Biogeogr. 26, 347–358 (2017).
    Article  Google Scholar 

    68.
    Nord, A. & Nilsson, J. Å. Heat dissipation rate constrains reproductive investment in a wild bird. Funct. Ecol. 33, 250–259 (2019).
    Article  Google Scholar 

    69.
    Cloete, S. W. P. et al. Variance components for live weight, body measurements and reproductive traits of pair-mated ostrich females. Br. Poult. Sci. 47, 147–158 (2006).
    CAS  PubMed  Article  Google Scholar 

    70.
    Rybnik, P. K., Horbanczuk, J. O., Naranowicz, H., Lukaszewicz, E. & Malecki, I. A. Semen collection in the ostrich (Struthio camelus) using a dummy or a teaser female. Br. Poult. Sci. 48, 635–643 (2007).
    CAS  PubMed  Article  Google Scholar 

    71.
    Brand, T. S., Olivier, T. R. & Gous, R. M. The response in food intake and reproductive parameters of breeding ostriches to increasing dietary energy. South Afr. J. Anim. Sci. 40, 434–437 (2010).
    Google Scholar 

    72.
    Brand, T. S., Olivier, T. R. & Gous, R. M. The reproductive response of female ostriches to dietary protein. Br. Poult. Sci. 56, 232–238 (2015).
    CAS  PubMed  Article  Google Scholar 

    73.
    Martin, P. A., Reimers, T. J., Lodge, J. R. & Dziuk, P. J. The effect of ratios and numbers of spermatozoa mixed from two males on proportions of offspring. J. Reprod. Fertil. 39, 251–258 (1974).
    CAS  PubMed  Article  Google Scholar 

    74.
    Birkhead, T. R. & Møller, A. P. Sperm Competition and Sexual Selection (Academic Press, 1998).

    75.
    Birkhead, T. R. & Biggins, J. D. Sperm competition mechanisms in birds: models and data. Behav. Ecol. 9, 253–260 (1998).
    Article  Google Scholar 

    76.
    Soley, J. T. & Roberts, J. C. Ultrastructure of ostrich (Struthio camelus) spermatozoa. II. Scanning electron microscopy. Onderstepoort J. Vet. Res. 61, 239–246 (1994).
    CAS  PubMed  Google Scholar 

    77.
    Lake, P. E. & Stewart, J. M. Artificial Insemination in Poultry. Ministry of Agriculture Fisheries and Food, Bulletin 213 (Her Majesty’s Stationery Office, 1978).

    78.
    Bonato, M., Malecki, I. A., Rybnik-Trzaskowska, P. K., Cornwallis, C. K. & Cloete, S. W. P. Predicting ejaculate quality and libido in male ostriches: effect of season and age. Anim. Reprod. Sci. 151, 49–55 (2014).
    PubMed  Article  Google Scholar 

    79.
    Bonato, M., Rybnik, P. K., Malecki, I. A., Cornwallis, C. K. & Cloete, S. W. P. Twice daily collection yields greater semen output and does not affect male libido in the ostrich. Anim. Reprod. Sci. 123, 258–264 (2011).
    PubMed  Article  Google Scholar 

    80.
    Muvhali, P. T. et al. Ostrich ejaculate characteristics and male libido around equinox and solstice dates. Trop. Anim. Health and Prod. 52, 2609–2619 (2020).
    CAS  Article  Google Scholar 

    81.
    Brand, Z., Cloete, S. W. P., Brown, C. R. & Malecki, I. A. Systematic factors that affect ostrich egg incubation traits. South Afr. J. Anim. Sci. 38, 315–325 (2008).
    Google Scholar 

    82.
    Bronneberg, R. G. G. et al. The relation between ultrasonographic observations in the oviduct and plasma progesterone, luteinizing hormone and estradiol during the egg laying cycle in ostriches. Domest. Anim. Endocrinol. 32, 15–28 (2007).
    CAS  PubMed  Article  Google Scholar 

    83.
    Van Schalkwyk, S. J., Cloete, S. W. P. & De Kock, J. A. Repeatability and phenotypic correlations for body weight and reproduction in commercial ostrich breeding pairs. Br. Poult. Sci. 37, 953–962 (1996).
    PubMed  Article  Google Scholar 

    84.
    Jones, R. C. & Lin, M. Spermatogenesis in birds. In Oxford Reviews of Reproductive Biology, Vol. 15 (ed. Milligan, S. R.) (Oxford University Press, 1993).

    85.
    R Core Team. R: A Language and Environment for Statistical Computing (R Core Team, 2020).

    86.
    Hadfield, J. D. MCMC methods for multi-response generalized linear mixed models: the MCMCglmm R package. J. Stat. Softw. 33, 1–22 (2010).
    Article  Google Scholar 

    87.
    Araya-Ajoy, Y. G. & Dingemanse, N. J. Repeatability, heritability, and age-dependence of seasonal plasticity in aggressiveness in a wild passerine bird. J. Anim. Ecol. 86, 227–238 (2017).
    PubMed  Article  Google Scholar 

    88.
    Araya-Ajoy, Y. G., Mathot, K. J. & Dingemanse, N. J. An approach to estimate short-term, long-term and reaction norm repeatability. Methods Ecol. Evol. 6, 1462–1473 (2015).
    Article  Google Scholar 

    89.
    Scheiner, S. M. Genetics and evolution of phenotypic plasticity. Annu. Rev. Ecol. Syst. 24, 35–68 (1993).
    Article  Google Scholar 

    90.
    Wilson, A. J. Why h2 does not always equal VA/VP. J. Evol. Biol. 21, 647–650 (2008).
    CAS  PubMed  Article  Google Scholar 

    91.
    de Villemereuil, P., Morrissey, M. B., Nakagawa, S. & Schielzeth, H. Fixed-effect variance and the estimation of repeatabilities and heritabilities: Issues and solutions. J. Evol. Biol. 31, 621–632 (2018).
    PubMed  Article  Google Scholar 

    92.
    de Villemereuil, P., Schielzeth, H., Nakagawa, S. & Morrissey, M. General methods for evolutionary quantitative genetic inference from generalized mixed models. Genetics 204, 1281–1294 (2016).
    PubMed  PubMed Central  Article  Google Scholar 

    93.
    BirdLife International. BirdLife International and Handbook of the Birds of the World. Bird Species Distribution Maps of the World (BirdLife International, 2019).

    94.
    Fick, S. E. & Hijmans, R. J. WorldClim 2: new 1-km spatial resolution climate surfaces for global land areas. Int. J. Climatol. 37, 4302–4315 (2017).
    Article  Google Scholar  More

  • in

    Genomic evidence of prevalent hybridization throughout the evolutionary history of the fig-wasp pollination mutualism

    1.
    Taylor, S. A. & Larson, E. L. Insights from genomes into the evolutionary importance and prevalence of hybridization in nature. Nat. Ecol. Evol. 3, 170–177 (2019).
    PubMed  Article  PubMed Central  Google Scholar 
    2.
    Payseur, B. A. & Rieseberg, L. H. A genomic perspective on hybridization and speciation. Mol. Ecol. 25, 2337–2360 (2016).
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    3.
    Arnold, M. L. & Kunte, K. Adaptive genetic exchange: a tangled history of admixture and evolutionary innovation. Trends Ecol. Evol. 32, 601–611 (2017).
    PubMed  Article  Google Scholar 

    4.
    Mallet, J. Hybrid speciation. Nature 446, 279–283 (2007).
    ADS  CAS  PubMed  Article  PubMed Central  Google Scholar 

    5.
    Abbott, R. et al. Hybridization and speciation. J. Evol. Biol. 26, 229–246 (2013).
    CAS  PubMed  Article  Google Scholar 

    6.
    Gross, B. L. & Rieseberg, L. H. The ecological genetics of homoploid hybrid speciation. J. Hered. 96, 241–252 (2005).
    CAS  PubMed  Article  Google Scholar 

    7.
    Schumer, M., Rosenthal, G. G. & Andolfatto, P. How common is homoploid hybrid speciation? Evolution 68, 1553–1560 (2014).
    PubMed  Article  Google Scholar 

    8.
    Grant, V. Pollination systems as isolating mechanisms in angiosperms. Evolution 3, 82–97 (1949).
    CAS  PubMed  Article  Google Scholar 

    9.
    Kay, K. M. & Sargent, R. D. The role of animal pollination in plant speciation: Integrating ecology, geography, and genetics. Annu. Rev. Ecol. Evol. Syst. 40, 637–656 (2009).
    Article  Google Scholar 

    10.
    Serrano-Serrano, M. L., Rolland, J., Clark, J. L., Salamin, N. & Perret, M. Hummingbird pollination and the diversification of angiosperms: an old and successful association in Gesneriaceae. Proc. R. Soc. B Biol. Sci. 284, https://doi.org/10.1098/rspb.2016.2816 (2017).

    11.
    Thompson, J. N. Specific hypotheses on the geographic mosaic of coevolution. Am. Nat. 153, S1–S14 (1999).
    Article  Google Scholar 

    12.
    Van der Niet, T., Peakall, R. & Johnson, S. D. Pollinator-driven ecological speciation in plants: new evidence and future perspectives. Ann. Bot. 113, 199–211 (2014).
    PubMed  PubMed Central  Article  Google Scholar 

    13.
    Armbruster, W. S. The specialization continuum in pollination systems: diversity of concepts and implications for ecology, evolution and conservation. Funct. Ecol. 31, 88–100 (2017).
    Article  Google Scholar 

    14.
    Ayasse, M., Stokl, J. & Francke, W. Chemical ecology and pollinator-driven speciation in sexually deceptive orchids. Phytochemistry 72, 1667–1677 (2011).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    15.
    Machado, C. A., Robbins, N., Gilbert, M. T. P. & Herre, E. A. Critical review of host specificity and its coevolutionary implications in the fig/fig-wasp mutualism. Proc. Natl Acad. Sci. USA 102, 6558–6565 (2005).
    ADS  CAS  PubMed  Article  Google Scholar 

    16.
    Kawakita, A. Evolution of obligate pollination mutualism in the tribe Phyllantheae (Phyllanthaceae). Plant Species Biol. 25, 3–19 (2010).
    Article  Google Scholar 

    17.
    Ramirez, W. Host specificity of fig wasps (Agaonidae). Evolution 24, 680–691 (1970).
    Article  Google Scholar 

    18.
    Schiestl, F. P. & Schluter, P. M. Floral isolation, specialized pollination, and pollinator behavior in orchids. Annu. Rev. Entomol. 54, 425–446 (2009).
    CAS  PubMed  Article  Google Scholar 

    19.
    Ramirez, S. R. et al. Asynchronous diversification in a specialized plant-pollinator mutualism. Science 333, 1742–1746 (2011).
    ADS  CAS  PubMed  Article  Google Scholar 

    20.
    Cruaud, A. et al. An extreme case of plant-insect co-diversification: figs and fig-pollinating wasps. Syst. Biol. 61, 1029–1047 (2012).
    PubMed  PubMed Central  Article  Google Scholar 

    21.
    Berg, C. C. & Corner, E. J. H. in Flora Malesiana Series I -Seed Plants Vol. 17 (ed. Nooteboom, H. P.) 1–702 (Nationaal Herbarium, Nederland, 2005).

    22.
    Wang, G., Cannon, C. H. & Chen, J. Pollinator sharing and gene flow among closely related sympatric dioecious fig taxa. Proc. R. Soc. B Biol. Sci. 283, https://doi.org/10.1098/rspb.2015.2963 (2016).

    23.
    Machado, C. A., Jousselin, E., Kjellberg, F., Compton, S. G. & Herre, E. A. Phylogenetic relationships, historical biogeography and character evolution of fig-pollinating wasps. Proc. R. Soc. B Biol. Sci. 268, 685–694 (2001).
    CAS  Article  Google Scholar 

    24.
    Harrison, R. D. Figs and the diversity of tropical rainforests. Bioscience 55, 1053–1064 (2005).
    Article  Google Scholar 

    25.
    Grison-Pigé, L., Bessière, J. M. & Hossaert-McKey, M. Specific attraction of fig-pollinating wasps: Role of volatile compounds released by tropical figs. J. Chem. Ecol. 28, 283–295 (2002).
    PubMed  Article  PubMed Central  Google Scholar 

    26.
    Herre, E. A. et al. Molecular phylogenies of figs and their pollinator wasps. J. Biogeogr. 23, 521–530 (1996).
    Article  Google Scholar 

    27.
    Molbo, D., Machado, C. A., Sevenster, J. G., Keller, L. & Herre, E. A. Cryptic species of fig-pollinating wasps: Implications for the evolution of the fig-wasp mutualism, sex allocation, and precision of adaptation. Proc. Natl Acad. Sci. USA 100, 5867–5872 (2003).
    ADS  CAS  PubMed  Article  PubMed Central  Google Scholar 

    28.
    Rasplus, J. Y. in The Biodiversity of African Plants (eds van der Maesen, L. J. G. et al.) 639–649 (Springer, 1996).

    29.
    Yang, L.-Y. et al. The incidence and pattern of co-pollinator diversification in dioecious and monoecious figs. Evolution 69, 294–304 (2015).
    PubMed  PubMed Central  Article  Google Scholar 

    30.
    Cornille, A. et al. Floral volatiles, pollinator sharing and diversification in the fig-wasp mutualism: insights from Ficus natalensis, and its two wasp pollinators (South Africa). Proc. R. Soc. B Biol. Sci. 279, 1731–1739 (2012).
    CAS  Article  Google Scholar 

    31.
    Compton, S. G. A collapse of host specificity in some African fig wasps. S. Afr. J. Sci. 86, 39–40 (1990).
    Google Scholar 

    32.
    Renoult, J. P., Kjellberg, F., Grout, C., Santoni, S. & Khadari, B. Cyto-nuclear discordance in the phylogeny of Ficus section Galoglychia and host shifts in plant-pollinator associations. BMC Evol. Biol. 9, 248 (2009).
    PubMed  PubMed Central  Article  CAS  Google Scholar 

    33.
    Satler, J. D. et al. Inferring processes of coevolutionary diversification in a community of Panamanian strangler figs and associated pollinating wasps. Evolution 73, 2295–2311 (2019).

    34.
    Jackson, A. P., Machado, C. A., Robbins, N. & Herre, E. A. Multi-locus phylogenetic analysis of neotropical figs does not support co-speciation with the pollinators: the importance of systematic scale in fig/wasp cophylogenetic studies. Symbiosis 45, 57–72 (2008).
    CAS  Google Scholar 

    35.
    Parrish, T. L., Koelewijn, H. P., van Dijk, P. J. & Kruijt, M. Genetic evidence for natural hybridization between species of dioecious Ficus on island populations. Biotropica 35, 333–343 (2003).
    Article  Google Scholar 

    36.
    Ramirez, W. Hybridization of Ficus religiosa with F. septica and F. aurea (Moraceae). Rev. Biol. Trop. 42, 339–342 (1994).
    Google Scholar 

    37.
    Wei, Z. D., Kobmoo, N., Cruaud, A. & Kjellberg, F. Genetic structure and hybridization in the species group of Ficus auriculata: can closely related sympatric Ficus species retain their genetic identity while sharing pollinators? Mol. Ecol. 23, 3538–3550 (2014).
    PubMed  Article  PubMed Central  Google Scholar 

    38.
    Bruun-Lund, S., Clement, W. L., Kjellberg, F. & Rønsted, N. First plastid phylogenomic study reveals potential cyto-nuclear discordance in the evolutionary history of Ficus L. (Moraceae). Mol. Phylogenet. Evol. 109, 93–104 (2017).
    PubMed  Article  Google Scholar 

    39.
    Zhang, X. et al. Genomes of the Banyan tree and pollinator wasp provide insights into fig-wasp coevolution. Cell 183, 875–889 (2020).
    CAS  PubMed  Article  Google Scholar 

    40.
    Mirarab, S. & Warnow, T. ASTRAL-II: coalescent-based species tree estimation with many hundreds of taxa and thousands of genes. Bioinformatics 31, 44–52 (2015).
    Article  CAS  Google Scholar 

    41.
    Rønsted, N., Weiblen, G. D., Clement, W. L., Zerega, N. J. C. & Savolainen, V. Reconstructing the phylogeny of figs (Ficus, Moraceae) to reveal the history of the fig pollination mutualism. Symbiosis 45, 45–55 (2008).
    Google Scholar 

    42.
    Ane, C., Larget, B., Baum, D. A., Smith, S. D. & Rokas, A. Bayesian estimation of concordance among gene trees. Mol. Biol. Evol. 24, 412–426 (2007).
    CAS  PubMed  Article  Google Scholar 

    43.
    Larget, B. R., Kotha, S. K., Dewey, C. N. & Ane, C. BUCKy: Gene tree/species tree reconciliation with Bayesian concordance analysis. Bioinformatics 26, 2910–2911 (2010).
    CAS  PubMed  Article  Google Scholar 

    44.
    Baum, D. A. Concordance trees, concordance factors, and the exploration of reticulate genealogy. Taxon 56, 417–426 (2007).
    Article  Google Scholar 

    45.
    Solis-Lemus, C., Bastide, P. & Ane, C. PhyloNetworks: a package for phylogenetic networks. Mol. Biol. Evol. 34, 3292–3298 (2017).
    CAS  PubMed  Article  Google Scholar 

    46.
    Soraggi, S., Wiuf, C. & Albrechtsen, A. Powerful inference with the D-statistic on low-coverage whole-genome data. G3 (Bethesda) 8, 551–566 (2018).

    47.
    Durand, E. Y., Patterson, N., Reich, D. & Slatkin, M. Testing for ancient admixture between closely related populations. Mol. Biol. Evol. 28, 2239–2252 (2011).
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    48.
    Degnan, J. H. & Rosenberg, N. A. Gene tree discordance, phylogenetic inference and the multispecies coalescent. Trends Ecol. Evol. 24, 332–340 (2009).
    PubMed  Article  Google Scholar 

    49.
    Conow, C., Fielder, D., Ovadia, Y. & Libeskind-Hadas, R. Jane: a new tool for the cophylogeny reconstruction problem. Algorithms Mol. Biol. 5, https://doi.org/10.1186/1748-7188-5-16 (2010).

    50.
    Ramsey, A. J. & Mandel, J. R. When one genome is not enough: organellar heteroplasmy in plants. Annual Plant Reviews 2, 619–658 (2019).
    Article  Google Scholar 

    51.
    Zhang, Q. & Liu, Y. & Sodmergen. Examination of the cytoplasmic DNA in male reproductive cells to determine the potential for cytoplasmic inheritance in 295 angiosperm species. Plant Cell Physiol. 44, 941–951 (2003).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    52.
    Hu, Y. C., Zhang, Q. & Rao, G. Y. & Sodmergen. Occurrence of plastids in the sperm cells of Caprifoliaceae: Biparental plastid inheritance in angiosperms is unilaterally derived from maternal inheritance. Plant Cell Physiol. 49, 958–968 (2008).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    53.
    Mayr, E. Animal Species and Evolution 1–811 (Belknap Press, 1963).

    54.
    Wu, C. I. The genic view of the process of speciation. J. Evol. Biol. 14, 851–865 (2001).
    Article  Google Scholar 

    55.
    Sun, M. et al. Deep phylogenetic incongruence in the angiosperm clade Rosidae. Mol. Phylogenet. Evol. 83, 156–166 (2015).
    PubMed  Article  PubMed Central  Google Scholar 

    56.
    Folk, R. A., Soltis, P. S., Soltis, D. E. & Guralnick, R. New prospects in the detection and comparative analysis of hybridization in the tree of life. Am. J. Bot. 105, 364–375 (2018).
    PubMed  Article  PubMed Central  Google Scholar 

    57.
    Jiao, X., Flouri, T., Rannala, B. & Yang, Z. The impact of cross-species gene flow on species tree estimation. Syst. Biol. 69, 830–847 (2020).

    58.
    Jousselin, E. et al. One fig to bind them all: host conservatism in a fig wasp community unraveled by cospeciation analyses among pollinating and nonpollinating fig wasps. Evolution 62, 1777–1797 (2008).
    PubMed  Article  PubMed Central  Google Scholar 

    59.
    Moe, A. M. & Weiblen, G. D. Pollinator-mediated reproductive isolation among dioecious fig species (Ficus, Moraceae). Evolution 66, 3710–3721 (2012).
    PubMed  Article  PubMed Central  Google Scholar 

    60.
    Wang, G., Compton, S. G. & Chen, J. The mechanism of pollinator specificity between two sympatric fig varieties: a combination of olfactory signals and contact cues. Ann. Bot. 111, 173–181 (2013).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    61.
    Bronstein, J. L. Maintenance of species-specificity in a neotropical fig – pollinator wasp mutualism. Oikos 48, 39–46 (1987).
    Article  Google Scholar 

    62.
    Ware, A., Kaye, P., Compton, S. & Noort, S. Fig volatiles: their role in attracting pollinators and maintaining pollinator specificity. Plant Syst. Evol. 186, 147–156 (1993).
    Article  Google Scholar 

    63.
    Soler, C. C. L., Proffit, M., Bessière, J. M., Hossaert-McKey, M. & Schatz, B. Evidence for intersexual chemical mimicry in a dioecious plant. Ecol. Lett. 15, 978–985 (2012).
    PubMed  Article  PubMed Central  Google Scholar 

    64.
    Hossaert-McKey, M., Soler, C., Schatz, B. & Proffit, M. Floral scents: their roles in nursery pollination mutualisms. Chemoecology 20, 75–88 (2010).
    Article  Google Scholar 

    65.
    Knudsen, J. T., Eriksson, R., Gershenzon, J. & Stahl, B. Diversity and distribution of floral scent. Bot. Rev. 72, 1–120 (2006).
    Article  Google Scholar 

    66.
    Herre, E. A., Jander, K. C. & Machado, C. A. Evolutionary ecology of figs and their associates: Recent progress and outstanding puzzles. Annu. Rev. Ecol. Evol. Syst. 39, 439–458 (2008).
    Article  Google Scholar 

    67.
    Kiester, A. R., Lande, R. & Schemske, D. W. Models of coevolution and speciation in plants and their pollinators. Am. Nat. 124, 220–243 (1984).
    Article  Google Scholar 

    68.
    Vereecken, N. J., Cozzolino, S. & Schiestl, F. P. Hybrid floral scent novelty drives pollinator shift in sexually deceptive orchids. BMC Evol. Biol. 10, 103 (2010).
    PubMed  PubMed Central  Article  CAS  Google Scholar 

    69.
    Rønsted, N. et al. 60 million years of co-divergence in the fig-wasp symbiosis. Proc. R. Soc. B Biol. Sci. 272, 0962–8452 (2005). 2593-2599.
    Google Scholar 

    70.
    Wiebes, J. T. Co-evolution of figs and their insect pollinators. Annu. Rev. Ecol. Syst. 10, 1–12 (1979).
    Article  Google Scholar 

    71.
    Zhu, H. et al. Native Seed Plants in Xishuangbanna of Yunnan (eds Zhu, H. & Yan, L.) 1–565 (Science Press, 2012).

    72.
    Yang, J. B., Li, D. Z. & Li, H. T. Highly effective sequencing whole chloroplast genomes of angiosperms by nine novel universal primer pairs. Mol. Ecol. Resour. 14, 1024–1031 (2014).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    73.
    Bolger, A. M., Lohse, M. & Usadel, B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30, 2114–2120 (2014).
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    74.
    Andrews, S. FastQC: a quality control tool for high throughput sequence data. http://www.bioinformatics.babraham.ac.uk/projects/fastqc/ (2010).

    75.
    Li, H. & Durbin, R. Fast and accurate long-read alignment with Burrows-Wheeler transform. Bioinformatics 26, 589–595 (2010).
    PubMed  PubMed Central  Article  CAS  Google Scholar 

    76.
    Li, H. et al. The sequence alignment/map format and SAMtools. Bioinformatics 25, 2078–2079 (2009).
    PubMed  PubMed Central  Article  CAS  Google Scholar 

    77.
    McKenna, A. et al. The genome analysis toolkit: a mapreduce framework for analyzing next-generation DNA sequencing data. Genome Res. 20, 1297–1303 (2010).
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    78.
    Jin, J.-J. et al. GetOrganelle: a fast and versatile toolkit for accurate de novo assembly of organelle genomes. Genome Biol. 21, 31 (2020).
    Article  Google Scholar 

    79.
    Wick, R. R., Schultz, M. B., Zobel, J. & Holt, K. E. Bandage: interactive visualization of de novo genome assemblies. Bioinformatics 31, 3350–3352 (2015).
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    80.
    Weiß, C. L., Pais, M., Cano, L. M., Kamoun, S. & Burbano, H. A. nQuire: a statistical framework for ploidy estimation using next generation sequencing. BMC Bioinformatics 19, 122 (2018).
    PubMed  PubMed Central  Article  CAS  Google Scholar 

    81.
    Stamatakis, A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30, 1312–1313 (2014).
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    82.
    Ronquist, F. et al. MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst. Biol. 61, 539–542 (2012).
    PubMed  PubMed Central  Article  Google Scholar 

    83.
    Yang, Z. H. PAML 4: phylogenetic analysis by maximum likelihood. Mol. Biol. Evol. 24, 1586–1591 (2007).
    CAS  PubMed  Article  Google Scholar 

    84.
    Zhu, T. Q., Dos Reis, M. & Yang, Z. H. Characterization of the uncertainty of divergence time estimation under relaxed molecular clock models using multiple loci. Syst. Biol. 64, 267–280 (2015).
    CAS  PubMed  Article  Google Scholar 

    85.
    Gardner, E. M., Sarraf, P., Williams, E. W. & Zerega, N. J. C. Phylogeny and biogeography of Maclura (Moraceae) and the origin of an anachronistic fruit. Mol. Phylogenet. Evol. 117, 49–59 (2017).
    PubMed  Article  Google Scholar 

    86.
    dos Reis, M. & Yang, Z. Approximate likelihood calculation on a phylogeny for bayesian estimation of divergence times. Mol. Biol. Evol. 28, 2161–2172 (2011).
    PubMed  Article  CAS  Google Scholar 

    87.
    Yang, Z. & Rannala, B. Bayesian estimation of species divergence times under a molecular clock using multiple fossil calibrations with soft bounds. Mol. Biol. Evol. 23, 212–226 (2006).
    CAS  PubMed  Article  Google Scholar 

    88.
    Matzke, N. J. Model selection in historical biogeography reveals that founder-event speciation is a crucial process in Island Clades. Syst. Biol. 63, 951–970 (2014).
    PubMed  Article  Google Scholar 

    89.
    Katoh, K. & Standley, D. M. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol. Biol. Evol. 30, 772–780 (2013).
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    90.
    Darriba, D., Taboada, G. L., Doallo, R. & Posada, D. jModelTest 2: more models, new heuristics and parallel computing. Nat. Methods 9, 772–772 (2012).
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    91.
    Price, M. N., Dehal, P. S. & Arkin, A. P. FastTree 2-approximately maximum-likelihood trees for large alignments. PLoS ONE 5, e9490 (2010).

    92.
    Korneliussen, T. S., Albrechtsen, A. & Nielsen, R. ANGSD: analysis of next generation sequencing data. BMC Bioinformatics 15, 1–13 (2014).
    Article  Google Scholar 

    93.
    Paradis, E., Claude, J. & Strimmer, K. APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20, 289–290 (2004).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    94.
    Wang, G. et al. Data from: Genomic evidence of prevalent hybridization throughout the evolutionary history of the fig-wasp pollination mutualism. Dryad, Dataset https://doi.org/10.5061/dryad.zcrjdfn7m (2020).

    95.
    Zhang, T. & Zhang, S. C. Code from: Genomic evidence of prevalent hybridization throughout the evolutionary history of the fig-wasp pollination mutualism. Github https://doi.org/10.5281/zenodo.4308886 (2020). More

  • in

    An evolving view on biogeochemical cycling of iron

    1.
    Ehrenberg, C. Vorläufige Mitteilungen über das wirkliche Vorkommen fossiler Infusorien und ihre große Verbreitung. Poggendorff Ann. 38, 213–227 (1836).
    Google Scholar 
    2.
    Chan, C. S. et al. The architecture of iron microbial mats reflects the adaptation of chemolithotrophic iron oxidation in freshwater and marine environments. Front. Microbiol. https://doi.org/10.3389/fmicb.2016.00796 (2016). Microscopic analysis indicates how the morphology of iron-oxidizing bacteria in microbial mats responds to environmental conditions.
    Article  PubMed  PubMed Central  Google Scholar 

    3.
    Melton, E. D., Swanner, E. D., Behrens, S., Schmidt, C. & Kappler, A. The interplay of microbially mediated and abiotic reactions in the biogeochemical Fe cycle. Nat. Rev. Microbiol. 12, 797–808 (2014).
    CAS  PubMed  Article  Google Scholar 

    4.
    Ehrlich, H. L., Newman, D. K. & Kappler, A. Ehrlich’s Geomicrobiology. (CRC Press, 2015).

    5.
    Byrne, J. M. et al. Redox cycling of Fe(II) and Fe(III) in magnetite by Fe-metabolizing bacteria. Science 347, 1473–1476 (2015). First article to demonstrate magnetite could support complete microbial iron cycling; that is, Fe(ii) in magnetite can be used as an electron source by Fe(ii) oxidizers and Fe(iii) can be used by Fe(iii) reducers as an electron acceptor in a cycling fashion.
    CAS  PubMed  Article  Google Scholar 

    6.
    Berg, J. S. et al. Intensive cryptic microbial iron cycling in the low iron water column of the meromictic Lake Cadagno. Environ. Microbiol. 18, 5288–5302 (2016).
    CAS  PubMed  Article  Google Scholar 

    7.
    Kappler, A. & Bryce, C. Cryptic biogeochemical cycles: unravelling hidden redox reactions. Environ. Microbiol. 19, 842–846 (2017).
    PubMed  Article  Google Scholar 

    8.
    Wang, M., Hu, R., Zhao, J., Kuzyakov, Y. & Liu, S. Iron oxidation affects nitrous oxide emissions via donating electrons to denitrification in paddy soils. Geoderma 271, 173–180 (2016).
    CAS  Article  Google Scholar 

    9.
    Beal, E. J., House, C. H. & Orphan, V. J. Manganese- and iron-dependent marine methane oxidation. Science 325, 184–187 (2009). First demonstration that methane oxidation can be coupled to reduction of iron(iii) oxides and manganese(iv) oxides.
    CAS  PubMed  Article  Google Scholar 

    10.
    Orihel, D. M. et al. The “nutrient pump:” iron-poor sediments fuel low nitrogen-to-phosphorus ratios and cyanobacterial blooms in polymictic lakes. Limnol. Oceanogr. 60, 856–871 (2015).
    Article  Google Scholar 

    11.
    Lalonde, K., Mucci, A., Ouellet, A. & Gélinas, Y. Preservation of organic matter in sediments promoted by iron. Nature 483, 198–200 (2012).
    CAS  PubMed  Article  Google Scholar 

    12.
    Muehe, E. M. et al. Fate of Cd during microbial Fe(III) mineral reduction by a novel and Cd-tolerant Geobacter species. Environ. Sci. Technol. 47, 14099–14109 (2013).
    CAS  PubMed  Article  Google Scholar 

    13.
    Glodowska, M. et al. Role of in situ natural organic matter in mobilizing As during microbial reduction of FeIII-mineral-bearing aquifer sediments from Hanoi (Vietnam). Environ. Sci. Technol. 54, 4149–4159 (2020).
    CAS  PubMed  Article  Google Scholar 

    14.
    Cutting, R. S., Coker, V. S., Fellowes, J. W., Lloyd, J. R. & Vaughan, D. J. Mineralogical and morphological constraints on the reduction of Fe(III) minerals by Geobacter sulfurreducens. Geochim. Cosmochim. Acta 73, 4004–4022 (2009).
    CAS  Article  Google Scholar 

    15.
    Wu, T. et al. Interactions between Fe(III)-oxides and Fe(III)-phyllosilicates during microbial reduction 2: natural subsurface sediments. Geomicrobiol. J. 34, 231–241 (2017).
    CAS  Article  Google Scholar 

    16.
    Jaisi, D. P., Dong, H. & Liu, C. Influence of biogenic Fe(II) on the extent of microbial reduction of Fe(III) in clay minerals nontronite, illite, and chlorite. Geochim. Cosmochim. Acta 71, 1145–1158 (2007).
    CAS  Article  Google Scholar 

    17.
    Bosch, J., Heister, K., Hofmann, T. & Meckenstock, R. U. Nanosized iron oxide colloids strongly enhance microbial iron reduction. Appl. Environ. Microbiol. 76, 184–189 (2010).
    CAS  PubMed  Article  Google Scholar 

    18.
    Aeppli, M. et al. Decreases in iron oxide reducibility during microbial reductive dissolution and transformation of ferrihydrite. Environ. Sci. Technol. 53, 8736–8746 (2019).
    CAS  PubMed  Article  Google Scholar 

    19.
    Levar, C. E., Hoffman, C. L., Dunshee, A. J., Toner, B. M. & Bond, D. R. Redox potential as a master variable controlling pathways of metal reduction by Geobacter sulfurreducens. ISME J. 11, 741–752 (2017).
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    20.
    Wang, Z. et al. Kinetics of reduction of Fe(III) complexes by outer membrane cytochromes MtrC and OmcA of Shewanella oneidensis MR-1. Appl. Environ. Microbiol. 74, 6746–6755 (2008).
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    21.
    Kügler, S. et al. Iron-organic matter complexes accelerate microbial iron cycling in an iron-rich Fen. Sci. Total. Environ. 646, 972–988 (2019).
    PubMed  Article  CAS  Google Scholar 

    22.
    Daugherty, E. E., Gilbert, B., Nico, P. S. & Borch, T. Complexation and redox buffering of iron(II) by dissolved organic matter. Environ. Sci. Technol. 51, 11096–11104 (2017).
    CAS  PubMed  Article  Google Scholar 

    23.
    von der Heyden, B., Roychoudhury, A. & Myneni, S. Iron-rich nanoparticles in natural aquatic environments. Minerals 9, 287 (2019). Thorough review of the nature and impact of iron nanoparticles in the environment.
    Article  CAS  Google Scholar 

    24.
    Hassellöv, M. & von der Kammer, F. Iron oxides as geochemical nanovectors for metal transport in soil-river systems. Elements 4, 401–406 (2008).
    Article  CAS  Google Scholar 

    25.
    Liu, J. et al. Particle size effect and the mechanism of hematite reduction by the outer membrane cytochrome OmcA of Shewanella oneidensis MR-1. Geochim. Cosmochim. Acta 193, 160–175 (2016).
    CAS  Article  Google Scholar 

    26.
    Druschel, G. K., Emerson, D., Sutka, R., Suchecki, P. & Luther, G. W. Low-oxygen and chemical kinetic constraints on the geochemical niche of neutrophilic iron(II) oxidizing microorganisms. Geochim. Cosmochim. Acta 72, 3358–3370 (2008). Landmark study using voltammetric electrodes to elucidate the optimum geochemical conditions of microaerophilic Fe(ii) oxidizers.
    CAS  Article  Google Scholar 

    27.
    Barnes, A., Sapsford, D. J., Dey, M. & Williams, K. P. Heterogeneous Fe(II) oxidation and zeta potential. J. Geochem. Explor. 100, 192–198 (2009).
    CAS  Article  Google Scholar 

    28.
    González-Davila, M., Santana-Casiano, J. M. & Millero, F. J. Oxidation of iron (II) nanomolar with H2O2 in seawater. Geochim. Cosmochim. Acta 69, 83–93 (2005).
    Article  CAS  Google Scholar 

    29.
    Kanzaki, Y. & Murakami, T. Rate law of Fe(II) oxidation under low O2 conditions. Geochim. Cosmochim. Acta 123, 338–350 (2013).
    CAS  Article  Google Scholar 

    30.
    King, D. W., Lounsbury, H. A. & Millero, F. J. Rates and mechanism of Fe(II) oxidation at nanomolar total iron concentrations. Environ. Sci. Technol. 29, 818–824 (1995).
    CAS  PubMed  Article  Google Scholar 

    31.
    Emerson, D., Fleming, E. J. & McBeth, J. M. Iron-oxidizing bacteria: an environmental and genomic perspective. Annu. Rev. Microbiol. 64, 561–583 (2010).
    CAS  PubMed  Article  Google Scholar 

    32.
    Chan, C. S., Emerson, D. & Luther, G. W. III The role of microaerophilic Fe-oxidizing micro-organisms in producing banded iron formations. Geobiology 14, 509–528 (2016).
    CAS  PubMed  Article  Google Scholar 

    33.
    Mori, J. F. et al. Physiological and ecological implications of an iron- or hydrogen-oxidizing member of the Zetaproteobacteria, Ghiorsea bivora, gen. nov., sp. nov. ISME J. 11, 2624–2636 (2017).
    PubMed  PubMed Central  Article  Google Scholar 

    34.
    Emerson, D. & De Vet, W. The role of FeOB in engineered water ecosystems: a review. J. AWWA 107, E47–E57 (2015).
    Article  Google Scholar 

    35.
    MacDonald, D. J. et al. Using in situ voltammetry as a tool to identify and characterize habitats of iron-oxidizing bacteria: from fresh water wetlands to hydrothermal vent sites. Environ. Sci. Process. Impacts 16, 2117–2126 (2014).
    PubMed  Article  Google Scholar 

    36.
    Emerson, D., Weiss, J. V. & Megonigal, J. P. Iron-oxidizing bacteria are associated with ferric hydroxide precipitates (Fe-plaque) on the roots of wetland plants. Appl. Environ. Microbiol. 65, 2758–2761 (1999).
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    37.
    Laufer, K. et al. Microaerophilic Fe(II)-oxidizing Zetaproteobacteria isolated from low-Fe marine coastal sediments: physiology and composition of their twisted stalks. Appl. Environ. Microbiol. 83, e03118–03116 (2017).
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    38.
    Orcutt, B. N. et al. Colonization of subsurface microbial observatories deployed in young ocean crust. ISME J. 5, 692–703 (2011).
    CAS  PubMed  Article  Google Scholar 

    39.
    Field, E. K. et al. Planktonic marine iron oxidizers drive iron mineralization under low-oxygen conditions. Geobiology 14, 499–508 (2016).
    CAS  PubMed  Article  Google Scholar 

    40.
    Maisch, M. et al. Contribution of microaerophilic iron(II)-oxidizers to iron(III) mineral formation. Environ. Sci. Technol. 53, 8197–8204 (2019).
    CAS  PubMed  Article  Google Scholar 

    41.
    Chiu, B. K., Kato, S., McAllister, S. M., Field, E. K. & Chan, C. S. Novel pelagic iron-oxidizing Zetaproteobacteria from the Chesapeake Bay oxic–anoxic transition zone. Front. Microbiol. 8, 1280 (2017).
    PubMed  PubMed Central  Article  Google Scholar 

    42.
    McAllister, S. M. et al. The Fe(II)-oxidizing Zetaproteobacteria: historical, ecological and genomic perspectives. FEMS Microbiol. Ecol. https://doi.org/10.1093/femsec/fiz015 (2019).
    Article  PubMed  PubMed Central  Google Scholar 

    43.
    Barco, R. A. et al. New insight into microbial iron oxidation as revealed by the proteomic profile of an obligate iron-oxidizing chemolithoautotroph. Appl. Environ. Microbiol. 81, 5927–5937 (2015).
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    44.
    McAllister, S. M. et al. Validating the Cyc2 neutrophilic iron oxidation pathway using meta-omics of Zetaproteobacteria iron mats at marine hydrothermal vents. mSystems 5, e00553–00519 (2020). Support for Cyc2 as the iron oxidase in microaerophilic Fe(ii) oxidizers.
    PubMed  PubMed Central  Article  Google Scholar 

    45.
    Jeans, C. et al. Cytochrome 572 is a conspicuous membrane protein with iron oxidation activity purified directly from a natural acidophilic microbial community. ISME J. 2, 542–550 (2008).
    CAS  PubMed  Article  Google Scholar 

    46.
    Edwards, B. A. & Ferris, F. G. Influence of water flow on in situ rates of bacterial Fe(II) oxidation. Geomicrobiol. J. 37, 67–75 (2020).
    CAS  Article  Google Scholar 

    47.
    Liu, J. 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. 3, 37 (2012).
    CAS  PubMed  PubMed Central  Google Scholar 

    48.
    Chan, C. S., McAllister, S. M., Garber, A., Hallahan, B. J. & Rozovsky, S. Fe oxidation by a fused cytochrome-porin common to diverse Fe-oxidizing bacteria. bioRxiv https://doi.org/10.1101/228056 (2018).
    Article  Google Scholar 

    49.
    Byrne, J. M., Schmidt, M., Gauger, T., Bryce, C. & Kappler, A. Imaging organic–mineral aggregates formed by Fe(II)-oxidizing bacteria using helium ion microscopy. Environ. Sci. Technol. Lett. 5, 209–213 (2018).
    CAS  Article  Google Scholar 

    50.
    Krepski, S. T., Emerson, D., Hredzak-Showalter, P. L., Luther, G. W. III & Chan, C. S. Morphology of biogenic iron oxides records microbial physiology and environmental conditions: toward interpreting iron microfossils. Geobiology 11, 457–471 (2013).
    CAS  PubMed  Article  Google Scholar 

    51.
    Sowers, T. D., Holden, K. L., Coward, E. K. & Sparks, D. L. Dissolved organic matter sorption and molecular fractionation by naturally occurring bacteriogenic iron (oxyhydr)oxides. Environ. Sci. Technol. 53, 4295–4304 (2019).
    CAS  PubMed  Article  Google Scholar 

    52.
    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. https://doi.org/10.1093/femsec/fix177 (2017).
    Article  Google Scholar 

    53.
    van der Grift, B., Rozemeijer, J. C., Griffioen, J. & van der Velde, Y. Iron oxidation kinetics and phosphate immobilization along the flow-path from groundwater into surface water. Hydrol. Earth Syst. Sci. 18, 4687–4702 (2014).
    Article  Google Scholar 

    54.
    Enright, A. M. L. & Ferris, F. G. Bacterial Fe(II) oxidation distinguished by long-range correlation in redox potential. J. Geophys. Res. Biogeosci. 121, 1249–1257 (2016).
    CAS  Article  Google Scholar 

    55.
    Lueder, U., Jørgensen, B. B., Kappler, A. & Schmidt, C. Photochemistry of iron in aquatic environments. Environ. Sci. Process. Impacts 22, 12–24 (2020).
    CAS  PubMed  Article  Google Scholar 

    56.
    Widdel, F. et al. Ferrous iron oxidation by anoxygenic phototrophic bacteria. Nature 362, 834–836 (1993).
    CAS  Article  Google Scholar 

    57.
    Hartman, H. The Evolution of Photosynthesis and Microbial Mats: A Speculation on the Banded Iron Formations. (Alan R. Liss, Inc., 1984).

    58.
    Ozaki, K., Tajika, E., Hong, P. K., Nakagawa, Y. & Reinhard, C. T. Effects of primitive photosynthesis on Earth’s early climate system. Nat. Geosci. 11, 55–59 (2018).
    CAS  Article  Google Scholar 

    59.
    Croal, L. R., Jiao, Y. & Newman, D. K. The fox operon from Rhodobacter strain SW2 promotes phototrophic Fe(II) oxidation in Rhodobacter capsulatus SB1003. J. Bacteriol. 189, 1774–1782 (2007).
    CAS  PubMed  Article  Google Scholar 

    60.
    Ehrenreich, A. & Widdel, F. Anaerobic oxidation of ferrous iron by purple bacteria, a new type of phototrophic metabolism. Appl. Environ. Microbiol. 60, 4517–4526 (1994).
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    61.
    Jiao, Y., Kappler, A., Croal, L. R. & Newman, D. K. Isolation and characterization of a genetically tractable photoautotrophic Fe(II)-oxidizing bacterium, Rhodopseudomonas palustris strain TIE-1. Appl. Environ. Microbiol. 71, 4487–4496 (2005).
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    62.
    Straub, K. L., Rainey, F. A. & Widdel, F. Rhodovulum iodosum sp. nov. and Rhodovulum robiginosum sp. nov., two new marine phototrophic ferrous-iron-oxidizing purple bacteria. Int. J. Syst. Evol. Microbiol. 49, 729–735 (1999).
    CAS  Article  Google Scholar 

    63.
    Heising, S., Richter, L., Ludwig, W. & Schink, B. Chlorobium ferrooxidans sp. nov., a phototrophic green sulfur bacterium that oxidizes ferrous iron in coculture with a Geospirillum sp. strain. Arch. Microbiol. 172, 116–124 (1999).
    CAS  PubMed  Article  Google Scholar 

    64.
    Llirós, M. et al. Pelagic photoferrotrophy and iron cycling in a modern ferruginous basin. Sci. Rep. 5, 13803 (2015).
    PubMed  PubMed Central  Article  Google Scholar 

    65.
    Laufer, K. et al. Physiological characterization of a halotolerant anoxygenic phototrophic Fe(II)-oxidizing green-sulfur bacterium isolated from a marine sediment. FEMS Microbiol. Ecol. https://doi.org/10.1093/femsec/fix054 (2017).
    Article  PubMed  Google Scholar 

    66.
    Jiao, Y. & Newman, D. K. The pio operon is essential for phototrophic Fe(II) oxidation in Rhodopseudomonas palustris TIE-1. J. Bacteriol. 189, 1765–1773 (2007).
    CAS  PubMed  Article  Google Scholar 

    67.
    Gupta, D. et al. Photoferrotrophs produce a PioAB electron conduit for extracellular electron uptake. mBio 10, e02668–02619 (2019).
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    68.
    Gledhill, M. & Buck, K. The organic complexation of iron in the marine environment: A review. Front. Microbiol. 3, 69 (2012).
    PubMed  PubMed Central  Google Scholar 

    69.
    Saraiva, I. H., Newman, D. K. & Louro, R. O. Functional characterization of the FoxE iron oxidoreductase from the photoferrotroph Rhodobacter ferrooxidans SW2. J. Biol. Chem. 287, 25541–25548 (2012).
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    70.
    Crowe, S. A. et al. Draft genome sequence of the pelagic photoferrotroph Chlorobium phaeoferrooxidans. Genome Announc. 5, e01584–01516 (2017).
    PubMed  PubMed Central  Article  Google Scholar 

    71.
    Bryce, C., Blackwell, N., Straub, D., Kleindienst, S. & Kappler, A. Draft genome sequence of Chlorobium sp. strain N1, a marine Fe(II)-oxidizing green sulfur bacterium. Microbiol. Resour. Announc. 8, e00080–00019 (2019).
    PubMed  PubMed Central  Article  Google Scholar 

    72.
    Miot, J. et al. Iron biomineralization by anaerobic neutrophilic iron-oxidizing bacteria. Geochim. Cosmochim. Acta 73, 696–711 (2009).
    CAS  Article  Google Scholar 

    73.
    Schaedler, S. et al. Formation of cell-iron-mineral aggregates by phototrophic and nitrate-reducing anaerobic Fe(II)-oxidizing bacteria. Geomicrobiol. J. 26, 93–103 (2009).
    CAS  Article  Google Scholar 

    74.
    Hegler, F., Schmidt, C., Schwarz, H. & Kappler, A. Does a low-pH microenvironment around phototrophic FeII-oxidizing bacteria prevent cell encrustation by FeIII minerals? FEMS Microbiol. Ecol. 74, 592–600 (2010).
    CAS  PubMed  Article  Google Scholar 

    75.
    Swanner, E. D. et al. Fractionation of Fe isotopes during Fe(II) oxidation by a marine photoferrotroph is controlled by the formation of organic Fe-complexes and colloidal Fe fractions. Geochim. Cosmochim. Acta 165, 44–61 (2015).
    CAS  Article  Google Scholar 

    76.
    Boyd, P. W. & Ellwood, M. J. The biogeochemical cycle of iron in the ocean. Nat. Geosci. 3, 675–682 (2010). A comprehensive review of the many dynamic processes which influence iron cycling in the oceans.
    CAS  Article  Google Scholar 

    77.
    Faust, B. C. & Zepp, R. G. Photochemistry of aqueous iron(III)-polycarboxylate complexes: roles in the chemistry of atmospheric and surface waters. Environ. Sci. Technol. 27, 2517–2522 (1993).
    CAS  Article  Google Scholar 

    78.
    Rose, A. L. & Waite, T. D. Reduction of organically complexed ferric iron by superoxide in a simulated natural water. Environ. Sci. Technol. 39, 2645–2650 (2005).
    CAS  PubMed  Article  Google Scholar 

    79.
    Voelker, B. M., Morel, F. M. M. & Sulzberger, B. Iron redox cycling in surface waters:  Effects of humic substances and light. Environ. Sci. Technol. 31, 1004–1011 (1997).
    CAS  Article  Google Scholar 

    80.
    Barbeau, K., Zhang, G., Live, D. H. & Butler, A. Petrobactin, a photoreactive siderophore produced by the oil-degrading marine bacterium Marinobacter hydrocarbonoclasticus. J. Am. Chem. Soc. 124, 378–379 (2002).
    CAS  PubMed  Article  Google Scholar 

    81.
    Waite, T. D. & Morel, F. M. M. Photoreductive dissolution of colloidal iron oxides in natural waters. Environ. Sci. Technol. 18, 860–868 (1984).
    CAS  PubMed  Article  Google Scholar 

    82.
    Sulzberger, B. Light-induced redox cycling of iron: roles for CO2 uptake and release by aquatic ecosystems. Aquat. Geochem. 21, 65–80 (2015).
    CAS  Article  Google Scholar 

    83.
    Garg, S., Rose, A. L. & Waite, T. D. Photochemical production of superoxide and hydrogen peroxide from natural organic matter. Geochim. Cosmochim. Acta 75, 4310–4320 (2011).
    CAS  Article  Google Scholar 

    84.
    Xing, G., Garg, S. & Waite, T. D. Is superoxide-mediated Fe(III) reduction important in sunlit surface waters? Environ. Sci. Technol. 53, 13179–13190 (2019).
    CAS  PubMed  Article  Google Scholar 

    85.
    Sutherland, K. M., Wankel, S. D. & Hansel, C. M. Dark biological superoxide production as a significant flux and sink of marine dissolved oxygen. Proc. Natl. Acad. Sci. USA 117, 3433–3439 (2020).
    CAS  PubMed  Article  Google Scholar 

    86.
    Diaz, J. M. et al. Widespread production of extracellular superoxide by heterotrophic bacteria. Science 340, 1223–1226 (2013).
    CAS  PubMed  Article  Google Scholar 

    87.
    Lis, H., Kranzler, C., Keren, N. & Shaked, Y. A comparative study of iron uptake rates and mechanisms amongst marine and fresh water cyanobacteria: prevalence of reductive iron uptake. Life 5, 841–860 (2015).
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    88.
    Swanner, E. D., Maisch, M., Wu, W. & Kappler, A. Oxic Fe(III) reduction could have generated Fe(II) in the photic zone of Precambrian seawater. Sci. Rep. 8, 4238 (2018).
    PubMed  PubMed Central  Article  CAS  Google Scholar 

    89.
    Emmenegger, L., Schönenberger, R., Sigg, L. & Sulzberger, B. Light-induced redox cycling of iron in circumneutral lakes. Limnol. Oceanogr. 46, 49–61 (2001).
    CAS  Article  Google Scholar 

    90.
    Lueder, U., Jørgensen, B. B., Kappler, A. & Schmidt, C. Fe(III) photoreduction producing Feaq2+ in oxic freshwater sediment. Environ. Sci. Technol. 54, 862–869 (2020).
    CAS  PubMed  Article  Google Scholar 

    91.
    Lueder, U. et al. Influence of physical perturbation on Fe(II) supply in coastal marine sediments. Environ. Sci. Technol. 54, 3209–3218 (2020).
    CAS  PubMed  Article  Google Scholar 

    92.
    Peng, C., Bryce, C., Sundman, A. & Kappler, A. Cryptic cycling of complexes containing Fe(III) and organic matter by phototrophic Fe(II)-oxidizing bacteria. Appl. Environ. Microbiol. 85, e02826–02818 (2019).
    CAS  PubMed  PubMed Central  Google Scholar 

    93.
    Schmidt, C., Behrens, S. & Kappler, A. Ecosystem functioning from a geomicrobiological perspective a conceptual framework for biogeochemical iron cycling. Environ. Chem. 7, 399–405 (2010).
    CAS  Article  Google Scholar 

    94.
    Raven, J. A., Kübler, J. E. & Beardall, J. Put out the light, and then put out the light. J. Mar. Biol. Assoc. U.K. 80, 1–25 (2000).
    CAS  Article  Google Scholar 

    95.
    Camacho, A., Walter, X. A., Picazo, A. & Zopfi, J. Photoferrotrophy: Remains of an ancient photosynthesis in modern environments. Front. Microbiol. 8 (2017). A review on the physiology of anoxygenic phototrophic Fe(ii) oxidizers and their role in modern and ancient redox-stratified systems.

    96.
    Crowe, S. A. et al. Deep-water anoxygenic photosythesis in a ferruginous chemocline. Geobiology 12, 322–339 (2014).
    CAS  PubMed  Article  Google Scholar 

    97.
    Straub, K. L., Benz, M., Schink, B. & Widdel, F. Anaerobic, nitrate-dependent microbial oxidation of ferrous iron. Appl. Environ. Microbiol. 62, 1458–1460 (1996).
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    98.
    Bryce, C. et al. Microbial anaerobic Fe(II) oxidation – Ecology, mechanisms and environmental implications. Environ. Microbiol. 20, 3462–3483 (2018).
    CAS  PubMed  Article  Google Scholar 

    99.
    Blöthe, M. & Roden, E. E. Composition and activity of an autotrophic Fe(II)-oxidizing, nitrate-reducing enrichment culture. Appl. Environ. Microbiol. 75, 6937–6940 (2009). Article describing the composition of the only confirmed autotrophic nitrate-dependent, Fe(ii)-oxidizing enrichment culture.
    PubMed  PubMed Central  Article  CAS  Google Scholar 

    100.
    Laufer, K., Røy, H., Jørgensen, B. B. & Kappler, A. Evidence for the existence of autotrophic nitrate-reducing Fe(II)-oxidizing bacteria in marine coastal sediment. Appl. Environ. Microbiol. 82, 6120–6131 (2016).
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    101.
    Liu, T., Chen, D., Luo, X., Li, X. & Li, F. Microbially mediated nitrate-reducing Fe(II) oxidation: quantification of chemodenitrification and biological reactions. Geochim. Cosmochim. Acta 256, 97–115 (2019).
    CAS  Article  Google Scholar 

    102.
    Otte, J. M. et al. N2O formation by nitrite-induced (chemo)denitrification in coastal marine sediment. Sci. Rep. 9, 10691 (2019).
    PubMed  PubMed Central  Article  CAS  Google Scholar 

    103.
    Wang, M., Hu, R., Ruser, R., Schmidt, C. & Kappler, A. Role of chemodenitrification for N2O emissions from nitrate reduction in rice paddy soils. ACS Earth Space Chem. 4, 122–132 (2020).
    CAS  Article  Google Scholar 

    104.
    He, S., Tominski, C., Kappler, A., Behrens, S. & Roden, E. E. Metagenomic analyses of the autotrophic Fe(II)-oxidizing, nitrate-reducing enrichment culture KS. Appl. Environ. Microbiol. 82, 2656–2668 (2016).
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    105.
    Buchwald, C., Grabb, K., Hansel, C. M. & Wankel, S. D. Constraining the role of iron in environmental nitrogen transformations: Dual stable isotope systematics of abiotic NO2− reduction by Fe(II) and its production of N2O. Geochim. Cosmochim. Acta 186, 1–12 (2016).
    CAS  Article  Google Scholar 

    106.
    Haaijer, S. C. M., Lamers, L. P. M., Smolders, A. J. P., Jetten, M. S. M. & Op den Camp, H. J. M. Iron sulfide and pyrite as potential electron donors for microbial nitrate reduction in freshwater wetlands. Geomicrobiol. J. 24, 391–401 (2007).
    CAS  Article  Google Scholar 

    107.
    Edwards, K. J., Rogers, D. R., Wirsen, C. O. & McCollom, T. M. Isolation and characterization of novel psychrophilic, neutrophilic, Fe-oxidizing, chemolithoautotrophic α- and γ-Proteobacteria from the deep sea. Appl. Environ. Microbiol. 69, 2906–2913 (2003).
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    108.
    Yan, R. et al. Effect of reduced sulfur species on chemolithoautotrophic pyrite oxidation with nitrate. Geomicrobiol. J. 36, 19–29 (2019).
    CAS  Article  Google Scholar 

    109.
    Holmes, P. R. & Crundwell, F. K. The kinetics of the oxidation of pyrite by ferric ions and dissolved oxygen: an electrochemical study. Geochim. Cosmochim. Acta 64, 263–274 (2000).
    CAS  Article  Google Scholar 

    110.
    Zhao, L., Dong, H., Edelmann, R. E., Zeng, Q. & Agrawal, A. Coupling of Fe(II) oxidation in illite with nitrate reduction and its role in clay mineral transformation. Geochim. Cosmochim. Acta 200, 353–366 (2017).
    CAS  Article  Google Scholar 

    111.
    Zhang, L., Dong, H., Kukkadapu, R. K., Jin, Q. & Kovarik, L. Electron transfer between sorbed Fe(II) and structural Fe(III) in smectites and its effect on nitrate-dependent iron oxidation by Pseudogulbenkiania sp. strain 2002. Geochim. Cosmochim. Acta 265, 132–147 (2019).
    CAS  Article  Google Scholar 

    112.
    Shelobolina, E. S., VanPraagh, C. G. & Lovley, D. R. Use of ferric and ferrous iron containing minerals for respiration by Desulfitobacterium frappieri. Geomicrobiol. J. 20, 143–156 (2003).
    CAS  Article  Google Scholar 

    113.
    Larese-Casanova, P., Haderlein, S. B. & Kappler, A. Biomineralization of lepidocrocite and goethite by nitrate-reducing Fe(II)-oxidizing bacteria: effect of pH, bicarbonate, phosphate, and humic acids. Geochim. Cosmochim. Acta 74, 3721–3734 (2010).
    CAS  Article  Google Scholar 

    114.
    Pantke, C. et al. Green rust formation during Fe(II) oxidation by the nitrate-reducing Acidovorax sp. strain BoFeN1. Environ. Sci. Technol. 46, 1439–1446 (2012).
    CAS  PubMed  Article  Google Scholar 

    115.
    Nordhoff, M. et al. Insights into nitrate-reducing Fe(II) oxidation mechanisms through analysis of cell-mineral associations, cell encrustation, and mineralogy in the chemolithoautotrophic enrichment culture KS. Appl. Environ. Microbiol. 83, e00752–00717 (2017).
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    116.
    Smith, R. L., Kent, D. B., Repert, D. A. & Böhlke, J. K. Anoxic nitrate reduction coupled with iron oxidation and attenuation of dissolved arsenic and phosphate in a sand and gravel aquifer. Geochim. Cosmochim. Acta 196, 102–120 (2017).
    CAS  Article  Google Scholar 

    117.
    Madison, A. S., Tebo, B. M., Mucci, A., Sundby, B. & Luther, G. W. Abundant porewater Mn(III) is a major component of the sedimentary redox system. Science 341, 875–878 (2013).
    CAS  PubMed  Article  Google Scholar 

    118.
    Gillispie, E. C., Taylor, S. E., Qafoku, N. P. & Hochella, M. F. Jr. Impact of iron and manganese nano-metal-oxides on contaminant interaction and fortification potential in agricultural systems – a review. Environ. Chem. 16, 377–390 (2019).
    CAS  Article  Google Scholar 

    119.
    Siebecker, M., Madison, A. S. & Luther, G. W. Reduction kinetics of polymeric (soluble) manganese (IV) oxide (MnO2) by ferrous iron (Fe2+). Aquat. Geochem. 21, 143–158 (2015).
    CAS  Article  Google Scholar 

    120.
    Herndon, E. M., Havig, J. R., Singer, D. M., McCormick, M. L. & Kump, L. R. Manganese and iron geochemistry in sediments underlying the redox-stratified Fayetteville Green Lake. Geochim. Cosmochim. Acta 231, 50–63 (2018).
    CAS  Article  Google Scholar 

    121.
    Maguffin, S. C. et al. Influence of manganese abundances on iron and arsenic solubility in rice paddy soils. Geochim. Cosmochim. Acta 276, 50–69 (2020).
    CAS  Article  Google Scholar 

    122.
    Lovley, D. R. & Phillips, E. J. P. Novel mode of microbial energy metabolism: Organic carbon oxidation coupled to dissimilatory reduction of iron or manganese. Appl. Environ. Microbiol. 54, 1472–1480 (1988).
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    123.
    Myers, C. R. & Nealson, K. H. Respiration-linked proton translocation coupled to anaerobic reduction of manganese(IV) and iron(III) in Shewanella putrefaciens MR-1. J. Bacteriol. 172, 6232–6238 (1990).
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    124.
    Lovley, D. R., Coates, J. D., Blunt-Harris, E. L., Phillips, E. J. P. & Woodward, J. C. Humic substances as electron acceptors for microbial respiration. Nature 382, 445–448 (1996).
    CAS  Article  Google Scholar 

    125.
    Coates, J. D., Ellis, D. J., Gaw, C. V. & Lovley, D. R. Geothrix fermentans gen. nov., sp. nov., a novel Fe(III)-reducing bacterium from a hydrocarbon-contaminated aquifer. Int. J. Syst. Evol. Microbiol. 49, 1615–1622 (1999).
    CAS  Article  Google Scholar 

    126.
    Tor, J. M. & Lovley, D. R. Anaerobic degradation of aromatic compounds coupled to Fe(III) reduction by Ferroglobus placidus. Environ. Microbiol. 3, 281–287 (2001).
    CAS  PubMed  Article  Google Scholar 

    127.
    Hansel, C. M., Benner, S. G. & Fendorf, S. Competing Fe(II)-induced mineralization pathways of ferrihydrite. Environ. Sci. Technol. 39, 7147–7153 (2005).
    CAS  PubMed  Article  Google Scholar 

    128.
    Shi, L. et al. The roles of outer membrane cytochromes of Shewanella and Geobacter in extracellular electron transfer. Environ. Microbiol. Rep. 1, 220–227 (2009).
    CAS  PubMed  Article  Google Scholar 

    129.
    Shi, L., Squier, T. C., Zachara, J. M. & Fredrickson, J. K. Respiration of metal (hydr)oxides by Shewanella and Geobacter: a key role for multihaem c-type cytochromes. Mol. Microbiol. 65, 12–20 (2007).
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    130.
    Butler, J. E., Young, N. D. & Lovley, D. R. Evolution of electron transfer out of the cell: comparative genomics of six Geobacter genomes. BMC Genomics 11, 40 (2010).
    PubMed  PubMed Central  Article  CAS  Google Scholar 

    131.
    Reguera, G. et al. Biofilm and nanowire production leads to increased current in Geobacter sulfurreducens fuel cells. Appl. Environ. Microbiol. 72, 7345–7348 (2006).
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    132.
    Lovley, D. R. & Holmes, D. E. Protein nanowires: the electrification of the microbial world and maybe our own. J. Bacteriol. 202, e00331–00320 (2020). A comprehensive and recent review on extracellular electron transfer by bacteria.
    CAS  PubMed  Article  Google Scholar 

    133.
    Reguera, G. et al. Extracellular electron transfer via microbial nanowires. Nature 435, 1098–1101 (2005).
    CAS  PubMed  Article  Google Scholar 

    134.
    Cologgi, D. L., Lampa-Pastirk, S., Speers, A. M., Kelly, S. D. & Reguera, G. Extracellular reduction of uranium via Geobacter conductive pili as a protective cellular mechanism. Proc. Natl. Acad. Sci. USA 108, 15248–15252 (2011).
    CAS  PubMed  Article  Google Scholar 

    135.
    Ueki, T. et al. Decorating the outer surface of microbially produced protein nanowires with peptides. ACS Synth. Biol. 8, 1809–1817 (2019).
    CAS  PubMed  Article  Google Scholar 

    136.
    Smith, J. A., Lovley, D. R. & Tremblay, P.-L. Outer cell surface components essential for Fe(III) oxide reduction by Geobacter metallireducens. Appl. Environ. Microbiol. 79, 901–907 (2013).
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    137.
    Pirbadian, S. et al. Shewanella oneidensis MR-1 nanowires are outer membrane and periplasmic extensions of the extracellular electron transport components. Proc. Natl. Acad. Sci. USA 111, 12883–12888 (2014).
    CAS  PubMed  Article  Google Scholar 

    138.
    El-Naggar, M. Y. et al. Electrical transport along bacterial nanowires from Shewanella oneidensis MR-1. Proc. Natl. Acad. Sci. USA 107, 18127–18131 (2010).
    CAS  PubMed  Article  Google Scholar 

    139.
    Roden, E. E. et al. Extracellular electron transfer through microbial reduction of solid-phase humic substances. Nat. Geosci. 3, 417–421 (2010).
    CAS  Article  Google Scholar 

    140.
    Lohmayer, R., Kappler, A., Lösekann-Behrens, T. & Planer-Friedrich, B. Sulfur species as redox partners and electron shuttles for ferrihydrite reduction by Sulfurospirillum deleyianum. Appl. Environ. Microbiol. 80, 3141–3149 (2014).
    PubMed  PubMed Central  Article  CAS  Google Scholar 

    141.
    Kappler, A., Benz, M., Schink, B. & Brune, A. Electron shuttling via humic acids in microbial iron(III) reduction in a freshwater sediment. FEMS Microbiol. Ecol. 47, 85–92 (2004).
    CAS  PubMed  Article  Google Scholar 

    142.
    Cervantes, F. J. et al. Reduction of humic substances by halorespiring, sulphate-reducing and methanogenic microorganisms. Environ. Microbiol. 4, 51–57 (2002).
    CAS  PubMed  Article  Google Scholar 

    143.
    Coates, J. D. et al. Recovery of humic-reducing bacteria from a diversity of environments. Appl. Environ. Microbiol. 64, 1504–1509 (1998).
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    144.
    Piepenbrock, A., Behrens, S. & Kappler, A. Comparison of humic substance- and Fe(III)-reducing microbial communities in anoxic aquifers. Geomicrobiol. J. 31, 917–928 (2014).
    CAS  Article  Google Scholar 

    145.
    Canfield, D. E. Reactive iron in marine sediments. Geochim. Cosmochim. Acta 53, 619–632 (1989).
    CAS  PubMed  Article  Google Scholar 

    146.
    Marsili, E. et al. Shewanella secretes flavins that mediate extracellular electron transfer. Proc. Natl. Acad. Sci. USA 105, 3968–3973 (2008).
    CAS  PubMed  Article  Google Scholar 

    147.
    von Canstein, H., Ogawa, J., Shimizu, S. & Lloyd, J. R. Secretion of flavins by Shewanella species and their role in extracellular electron transfer. Appl. Environ. Microbiol. 74, 615–623 (2008).
    Article  CAS  Google Scholar 

    148.
    Nevin, K. P. & Lovley, D. R. Mechanisms for Fe(III) oxide reduction in sedimentary environments. Geomicrobiol. J. 19, 141–159 (2002).
    CAS  Article  Google Scholar 

    149.
    Markelova, E. et al. Deconstructing the redox cascade: what role do microbial exudates (flavins) play? Environ. Chem. 14, 515–524 (2017).
    CAS  Article  Google Scholar 

    150.
    Bai, Y. et al. AQDS and redox-active NOM enables microbial Fe(III)-mineral reduction at cm-scales. Environ. Sci. Technol. 54, 4131–4139 (2020). The first article to demonstrate that microorganisms can transfer electrons to Fe(iii) over centimetre distances by electron shuttling.
    CAS  PubMed  Article  Google Scholar 

    151.
    Bai, Y., Sun, T., Angenent, L. T., Haderlein, S. B. & Kappler, A. Electron hopping enables rapid electron transfer between quinone-/hydroquinone-containing organic molecules in microbial iron(III) mineral reduction. Environ. Sci. Technol. 54, 10646–10653 (2020).
    CAS  PubMed  Article  Google Scholar 

    152.
    Liu, F. et al. Magnetite compensates for the lack of a pilin-associated c-type cytochrome in extracellular electron exchange. Environ. Microbiol. 17, 648–655 (2015).
    CAS  PubMed  Article  Google Scholar 

    153.
    Taillefert, M. et al. Shewanella putrefaciens produces an Fe(III)-solubilizing organic ligand during anaerobic respiration on insoluble Fe(III) oxides. J. Inorg. Biochem. 101, 1760–1767 (2007).
    CAS  PubMed  Article  Google Scholar 

    154.
    in ‘t Zandt, M. H., de Jong, A. E., Slomp, C. P. & Jetten, M. S. The hunt for the most-wanted chemolithoautotrophic spookmicrobes. FEMS Microbiol. Ecol. https://doi.org/10.1093/femsec/fiy064 (2018).
    Article  PubMed  PubMed Central  Google Scholar 

    155.
    Sivan, O. et al. Geochemical evidence for iron-mediated anaerobic oxidation of methane. Limnol. Oceanogr. 56, 1536–1544 (2011).
    CAS  Article  Google Scholar 

    156.
    Miura, Y., Watanabe, A., Murase, J. & Kimura, M. Methane production and its fate in paddy fields. Soil Sci. Plant Nutr. 38, 673–679 (1992).
    CAS  Article  Google Scholar 

    157.
    Crowe, S. A. et al. The methane cycle in ferruginous Lake Matano. Geobiology 9, 61–78 (2011).
    CAS  PubMed  Article  Google Scholar 

    158.
    Amos, R. T. et al. Evidence for iron-mediated anaerobic methane oxidation in a crude oil-contaminated aquifer. Geobiology 10, 506–517 (2012).
    CAS  PubMed  Article  Google Scholar 

    159.
    Glodowska, M. et al. Arsenic mobilization by anaerobic iron-dependent methane oxidation. Commun. Earth Environ. 1, 42 (2020). First study providing evidence that anaerobic oxidation of methane coupled to reduction of arsenic-bearing Fe(iii) minerals can lead to arsenic mobilization in groundwater.
    Article  Google Scholar 

    160.
    Scheller, S., Yu, H., Chadwick, G. L., McGlynn, S. E. & Orphan, V. J. Artificial electron acceptors decouple archaeal methane oxidation from sulfate reduction. Science 351, 703–707 (2016).
    CAS  PubMed  Article  Google Scholar 

    161.
    Wegener, G., Krukenberg, V., Riedel, D., Tegetmeyer, H. E. & Boetius, A. Intercellular wiring enables electron transfer between methanotrophic archaea and bacteria. Nature 526, 587–590 (2015).
    CAS  PubMed  Article  Google Scholar 

    162.
    Ettwig, K. F. et al. Archaea catalyze iron-dependent anaerobic oxidation of methane. Proc. Natl. Acad. Sci. USA 113, 12792–12796 (2016).
    CAS  PubMed  Article  Google Scholar 

    163.
    Cai, C. et al. A methanotrophic archaeon couples anaerobic oxidation of methane to Fe(III) reduction. ISME J. 12, 1929–1939 (2018).
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    164.
    Clément, J.-C., Shrestha, J., Ehrenfeld, J. G. & Jaffé, P. R. Ammonium oxidation coupled to dissimilatory reduction of iron under anaerobic conditions in wetland soils. Soil. Biol. Biochem. 37, 2323–2328 (2005).
    Article  CAS  Google Scholar 

    165.
    Huang, S. & Jaffé, P. R. Characterization of incubation experiments and development of an enrichment culture capable of ammonium oxidation under iron-reducing conditions. Biogeosciences 12, 769–779 (2015).
    Article  Google Scholar 

    166.
    Li, X. et al. Evidence of nitrogen loss from anaerobic ammonium oxidation coupled with ferric iron reduction in an intertidal wetland. Environ. Sci. Technol. 49, 11560–11568 (2015).
    CAS  PubMed  Article  Google Scholar 

    167.
    Zhou, G.-W. et al. Electron shuttles enhance anaerobic ammonium oxidation coupled to iron(III) reduction. Environ. Sci. Technol. 50, 9298–9307 (2016).
    CAS  PubMed  Article  Google Scholar 

    168.
    Yang, W. H., Weber, K. A. & Silver, W. L. Nitrogen loss from soil through anaerobic ammonium oxidation coupled to iron reduction. Nat. Geosci. 5, 538–541 (2012).
    CAS  Article  Google Scholar 

    169.
    Li, X. et al. Simultaneous Fe(III) reduction and ammonia oxidation process in Anammox sludge. J. Environ. Sci. 64, 42–50 (2018).
    Article  Google Scholar 

    170.
    Huang, S. & Jaffé, P. R. Isolation and characterization of an ammonium-oxidizing iron reducer: Acidimicrobiaceae sp. A6. PLoS ONE 13, e0194007 (2018).
    PubMed  PubMed Central  Article  CAS  Google Scholar 

    171.
    Sawayama, S. Possibility of anoxic ferric ammonium oxidation. J. Biosci. Bioeng. 101, 70–72 (2006).
    CAS  PubMed  Article  Google Scholar 

    172.
    Zhu, X., Burger, M., Doane, T. A. & Horwath, W. R. Ammonia oxidation pathways and nitrifier denitrification are significant sources of N2O and NO under low oxygen availability. Proc. Natl. Acad. Sci. USA 110, 6328–6333 (2013).
    CAS  PubMed  Article  Google Scholar 

    173.
    Ginn, B., Meile, C., Wilmoth, J., Tang, Y. & Thompson, A. Rapid iron reduction rates are stimulated by high-amplitude redox fluctuations in a tropical forest soil. Environ. Sci. Technol. 51, 3250–3259 (2017). A good example of the dynamic nature of iron cycling in the environment and its impact on the reducibility of minerals.
    CAS  PubMed  Article  Google Scholar 

    174.
    Mejia, J., Roden, E. E. & Ginder-Vogel, M. Influence of oxygen and nitrate on Fe (hydr)oxide mineral transformation and soil microbial communities during redox cycling. Environ. Sci. Technol. 50, 3580–3588 (2016).
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    175.
    Laufer, K. et al. Coexistence of microaerophilic, nitrate-reducing, and phototrophic Fe(II) oxidizers and Fe(III) reducers in coastal marine sediment. Appl. Environ. Microbiol. 82, 1433–1447 (2016).
    CAS  PubMed Central  Article  PubMed  Google Scholar 

    176.
    Hansel, C. M., Ferdelman, T. G. & Tebo, B. M. Cryptic cross-linkages among biogeochemical cycles: novel insights from reactive intermediates. Elements 11, 409–414 (2015). A review on cryptic element cycling in the environment, including cryptic iron cycling.
    CAS  Article  Google Scholar 

    177.
    Klueglein, N. & Kappler, A. Abiotic oxidation of Fe(II) by reactive nitrogen species in cultures of the nitrate-reducing Fe(II) oxidizer Acidovorax sp. BoFeN1 – questioning the existence of enzymatic Fe(II) oxidation. Geobiology 11, 180–190 (2013).
    CAS  PubMed  Article  Google Scholar 

    178.
    Matus, F. et al. Ferrous wheel hypothesis: Abiotic nitrate incorporation into dissolved organic matter. Geochim. Cosmochim. Acta 245, 514–524 (2019). Demonstration of the ‘ferrous wheel hypothesis’ with insights for the role of coupled iron and nitrogen cycling in the environment.
    CAS  Article  Google Scholar 

    179.
    Chen, C., Hall, S. J., Coward, E. & Thompson, A. Iron-mediated organic matter decomposition in humid soils can counteract protection. Nat. Commun. 11, 2255 (2020).
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    180.
    Patzner, M. S. et al. Iron mineral dissolution releases iron and associated organic carbon during permafrost thaw. Nat. Commun. 11, 6329 (2020).
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    181.
    Beckwith, C. R. et al. Characterization of MtoD from Sideroxydans lithotrophicus: a cytochrome c electron shuttle used in lithoautotrophic growth. Front. Microbiol. 6, 332 (2015).
    PubMed  PubMed Central  Article  Google Scholar 

    182.
    Bird, L. J., Bonnefoy, V. & Newman, D. K. Bioenergetic challenges of microbial iron metabolisms. Trends Microbiol. 19, 330–340 (2011).
    CAS  PubMed  Article  Google Scholar 

    183.
    Field, S. J. et al. Purification and magneto-optical spectroscopic characterization of cytoplasmic membrane and outer membrane multiheme c-type cytochromes from Shewanella frigidimarina NCIMB400. J. Biol. Chem. 275, 8515–8522 (2000).
    CAS  PubMed  Article  Google Scholar 

    184.
    Giffaut, E. et al. Andra thermodynamic database for performance assessment: ThermoChimie. Appl. Geochem. 49, 225–236 (2014).
    CAS  Article  Google Scholar 

    185.
    Salmon, T. P., Rose, A. L., Neilan, B. A. & Waite, T. D. The FeL model of iron acquisition: nondissociative reduction of ferric complexes in the marine environment. Limnol. Oceanogr. 51, 1744–1754 (2006).
    CAS  Article  Google Scholar 

    186.
    Navrotsky, A., Mazeina, L. & Majzlan, J. Size-driven structural and thermodynamic complexity in iron oxides. Science 319, 1635–1638 (2008).
    CAS  PubMed  Article  Google Scholar 

    187.
    Gorski, C. A., Edwards, R., Sander, M., Hofstetter, T. B. & Stewart, S. M. Thermodynamic characterization of iron oxide–aqueous Fe2+ redox couples. Environ. Sci. Technol. 50, 8538–8547 (2016). One of the first examples of using electrochemical methods to better understand the range of redox potentials present in different iron phases.
    CAS  PubMed  Article  Google Scholar 

    188.
    Robie, R. A. & Heminway, B. S. Thermodynamic properties of minerals and related substances at 298.15 K and 1 bar (105 pascals) pressure and at higher temperatures. (United States Printing Office, 1995).

    189.
    Navrotsky, A., Ma, C., Lilova, K. & Birkner, N. Nanophase transition metal oxides show large thermodynamically driven shifts in oxidation-reduction equilibria. Science 330, 199–201 (2010).
    CAS  PubMed  Article  Google Scholar 

    190.
    Robie, R. A. & Bethke, P. Molar Volumes and Densities of Minerals. Report TEI-822 (United States Department of the Interior Geological Survey, 1962).

    191.
    Gorski, C. A., Nurmi, J. T., Tratnyek, P. G., Hofstetter, T. B. & Scherer, M. M. Redox behavior of magnetite: implications for contaminant reduction. Environ. Sci. Technol. 44, 55–60 (2010).
    CAS  PubMed  Article  Google Scholar 

    192.
    Gorski, C. A., Klüpfel, L. E., Voegelin, A., Sander, M. & Hofstetter, T. B. Redox properties of structural Fe in clay minerals: 3. Relationships between smectite redox and structural properties. Environ. Sci. Technol. 47, 13477–13485 (2013).
    CAS  PubMed  Article  Google Scholar 

    193.
    Oswald, K. et al. Aerobic gammaproteobacterial methanotrophs mitigate methane emissions from oxic and anoxic lake waters. Limnol. Oceanogr. 61, S101–S118 (2016).
    Article  Google Scholar 

    194.
    Braunschweig, J., Bosch, J. & Meckenstock, R. U. Iron oxide nanoparticles in geomicrobiology: from biogeochemistry to bioremediation. N. Biotechnol. 30, 793–802 (2013).
    CAS  PubMed  Article  Google Scholar 

    195.
    Villa, R. D., Trovó, A. G. & Nogueira, R. F. P. Environmental implications of soil remediation using the Fenton process. Chemosphere 71, 43–50 (2008).
    CAS  PubMed  Article  Google Scholar 

    196.
    Wagai, R. & Mayer, L. M. Sorptive stabilization of organic matter in soils by hydrous iron oxides. Geochim. Cosmochim. Acta 71, 25–35 (2007).
    CAS  Article  Google Scholar 

    197.
    Nitzsche, K. S. et al. Arsenic removal from drinking water by a household sand filter in Vietnam — effect of filter usage practices on arsenic removal efficiency and microbiological water quality. Sci. Total. Environ. 502, 526–536 (2015).
    CAS  PubMed  Article  Google Scholar 

    198.
    Sipos, P., Németh, T., Kis, V. K. & Mohai, I. Sorption of copper, zinc and lead on soil mineral phases. Chemosphere 73, 461–469 (2008).
    CAS  PubMed  Article  Google Scholar 

    199.
    Poulton, S. W. & Canfield, D. E. Development of a sequential extraction procedure for iron: implications for iron partitioning in continentally derived particulates. Chem. Geol. 214, 209–221 (2005).
    CAS  Article  Google Scholar 

    200.
    Schaedler, F., Kappler, A. & Schmidt, C. A revised iron extraction protocol for environmental samples rich in nitrite and carbonate. Geomicrobiol. J. 35, 23–30 (2018).
    CAS  Article  Google Scholar 

    201.
    Porsch, K. & Kappler, A. FeII oxidation by molecular O2 during HCl extraction. Environ. Chem. 8, 190–197 (2011).
    CAS  Article  Google Scholar 

    202.
    Roden, E. E. & Zachara, J. M. Microbial reduction of crystalline iron(III) oxides:  Influence of oxide surface area and potential for cell growth. Environ. Sci. Technol. 30, 1618–1628 (1996).
    CAS  Article  Google Scholar 

    203.
    Tessier, A., Campbell, P. G. C. & Bisson, M. Sequential extraction procedure for the speciation of particulate trace metals. Anal. Chem. 51, 844–851 (1979).
    CAS  Article  Google Scholar 

    204.
    Stookey, L. L. Ferrozine – a new spectrophotometric reagent for iron. Anal. Chem. 42, 779–781 (1970).
    CAS  Article  Google Scholar 

    205.
    Clark, L. J. Iron(II) determination in the presence of iron(III) using 4,7-diphenyl-1,10-phenanthroline. Anal. Chem. 34, 348–352 (1962).
    CAS  Article  Google Scholar 

    206.
    Viollier, E., Inglett, P. W., Hunter, K., Roychoudhury, A. N. & Van Cappellen, P. The ferrozine method revisited: Fe(II)/Fe(III) determination in natural waters. Appl. Geochem. 15, 785–790 (2000).
    CAS  Article  Google Scholar  More

  • in

    Human disturbance causes widespread disruption of animal movement

    1.
    Newbold, T. et al. Global effects of land use on local terrestrial biodiversity. Nature 520, 45–50 (2015).
    CAS  PubMed  Google Scholar 
    2.
    Halpern, B. S. et al. A global map of human impact on marine ecosystems. Science 319, 948–952 (2008).
    CAS  PubMed  Google Scholar 

    3.
    Queiroz, N. et al. Global spatial risk assessment of sharks under the footprint of fisheries. Nature 572, 461–466 (2019).
    CAS  PubMed  Google Scholar 

    4.
    Tucker, M. A. et al. Moving in the anthropocene: global reductions in terrestrial mammalian movements. Science 359, 466–469 (2018).
    CAS  PubMed  Google Scholar 

    5.
    Wang, X. et al. Stochastic simulations reveal few green wave surfing populations among spring migrating herbivorous waterfowl. Nat. Commun. 10, 2187 (2019).
    PubMed  PubMed Central  Google Scholar 

    6.
    Fahrig, L. Non-optimal animal movement in human-altered landscapes. Funct. Ecol. 21, 1003–1015 (2007).
    Google Scholar 

    7.
    Cosgrove, A. J., McWhorter, T. J. & Maron, M. Consequences of impediments to animal movements at different scales: a conceptual framework and review. Divers. Distrib. 24, 448–459 (2018).
    Google Scholar 

    8.
    Mergey, M., Helder, R. & Roeder, J.-J. Effect of forest fragmentation on space-use patterns in the European pine marten (Martes martes). J. Mammal. 92, 328–335 (2011).
    Google Scholar 

    9.
    Main, M. T., Davis, R. A., Blake, D., Mills, H. & Doherty, T. S. Human impact overrides bioclimatic drivers of red fox home range size globally. Divers. Distrib. https://doi.org/10.1111/ddi.13115 (2020).

    10.
    Laver, P. N. & Alexander, K. A. Association with humans and seasonality interact to reverse predictions for animal space use. Mov. Ecol. 6, 5 (2018).
    PubMed  PubMed Central  Google Scholar 

    11.
    Riotte-Lambert, L. & Matthiopoulos, J. Environmental predictability as a cause and consequence of animal movement. Trends Ecol. Evol. 35, 163–174 (2020).
    PubMed  Google Scholar 

    12.
    Laurian, C., Ouellet, J.-P., Courtois, R., Breton, L. & St-Onge, S. Effects of intensive harvesting on moose reproduction. J. Appl. Ecol. 37, 515–531 (2000).
    Google Scholar 

    13.
    Tamburello, N., Côté, I. M. & Dulvy, N. K. Energy and the scaling of animal space use. Am. Nat. 186, 196–211 (2015).
    PubMed  Google Scholar 

    14.
    Jetz, W., Carbone, C., Fulford, J. & Brown, J. H. The scaling of animal space use. Science 306, 266–268 (2004).
    CAS  PubMed  Google Scholar 

    15.
    Perona, A. M., Urios, V. & López-López, P. Holidays? Not for all. Eagles have larger home ranges on holidays as a consequence of human disturbance. Biol. Conserv. 231, 59–66 (2019).
    Google Scholar 

    16.
    Staggenborg, J., Schaefer, H. M., Stange, C., Naef-Daenzer, B. & Grüebler, M. U. Time and travelling costs during chick-rearing in relation to habitat quality in little owls Athene noctua. Ibis (Lond. 1859) 159, 519–531 (2017).
    Google Scholar 

    17.
    Suraci, J. P., Clinchy, M., Zanette, L. Y. & Wilmers, C. C. Fear of humans as apex predators has landscape-scale impacts from mountain lions to mice. Ecol. Lett. 22, 1578–1586 (2019).
    PubMed  Google Scholar 

    18.
    Blomquist, S. & Hunter, M. L. Jr A multi-scale assessment of habitat selection and movement patterns by northern leopard frog (Lithobates [Rana] pipiens) in a managed forest. Herpetol. Conserv. Biol. 4, 142–160 (2009).
    Google Scholar 

    19.
    Peaden, J. M., Nowakowski, A. J., Tuberville, T. D., Buhlmann, K. A. & Todd, B. D. Effects of roads and roadside fencing on movements, space use, and carapace temperatures of a threatened tortoise. Biol. Conserv. 214, 13–22 (2017).
    Google Scholar 

    20.
    Siffczyk, C., Brotons, L., Kangas, K. & Orell, M. Home range size of willow tits: a response to winter habitat loss. Oecologia 136, 635–642 (2003).
    PubMed  Google Scholar 

    21.
    Breininger, D. R., Bolt, M. R., Legare, M. L., Drese, J. H. & Stolen, E. D. Factors influencing home-range sizes of eastern indigo snakes in central Florida. J. Herpetol. 45, 484–490 (2011).
    Google Scholar 

    22.
    Hirt, M. R., Jetz, W., Rall, B. C. & Brose, U. A general scaling law reveals why the largest animals are not the fastest. Nat. Ecol. Evol. 1, 1116–1122 (2017).
    PubMed  Google Scholar 

    23.
    Garland, T. & Albuquerque, R. L. Locomotion, energetics, performance, and behavior: a mammalian perspective on lizards, and vice versa. Integr. Comp. Biol. 57, 252–266 (2017).
    PubMed  Google Scholar 

    24.
    Wilson, K. S., Pond, B. A., Brown, G. S. & Schaefer, J. A. The biogeography of home range size of woodland caribou Rangifer tarandus caribou. Divers. Distrib. 25, 205–216 (2019).
    Google Scholar 

    25.
    Wang, Y., Smith, J. A. & Wilmers, C. C. Residential development alters behavior, movement, and energetics in a top carnivore. PLoS ONE 12, e0184687 (2017).
    PubMed  PubMed Central  Google Scholar 

    26.
    Vangestel, C., Braeckman, B. P., Matheve, H. & Lens, L. Constraints on home range behaviour affect nutritional condition in urban house sparrows (Passer domesticus). Biol. J. Linn. Soc. Lond. 101, 41–50 (2010).
    Google Scholar 

    27.
    Hinam, H. L. & St. Clair, C. C. High levels of habitat loss and fragmentation limit reproductive success by reducing home range size and provisioning rates of northern saw-whet owls. Biol. Conserv. 141, 524–535 (2008).
    Google Scholar 

    28.
    Herrera, J. M., de Sá Teixeira, I., Rodríguez-Pérez, J. & Mira, A. Landscape structure shapes carnivore-mediated seed dispersal kernels. Landsc. Ecol. 31, 731–743 (2016).
    Google Scholar 

    29.
    Carpenter, J. K., O’Donnell, C. F. J., Moltchanova, E. & Kelly, D. Long seed dispersal distances by an inquisitive flightless rail (Gallirallus australis) are reduced by interaction with humans. R. Soc. Open Sci. 6, 190397 (2019).
    PubMed  PubMed Central  Google Scholar 

    30.
    Januchowski-Hartley, F. A., Graham, N. A. J., Feary, D. A., Morove, T. & Cinner, J. E. Fear of fishers: human predation explains behavioral changes in coral reef fishes. PLoS ONE 6, e22761 (2011).
    CAS  PubMed  PubMed Central  Google Scholar 

    31.
    Whittington, J., Low, P. & Hunt, B. Temporal road closures improve habitat quality for wildlife. Sci. Rep. 9, 3772 (2019).
    PubMed  PubMed Central  Google Scholar 

    32.
    Soanes, K. et al. Movement re-established but not restored: inferring the effectiveness of road-crossing mitigation for a gliding mammal by monitoring use. Biol. Conserv. 159, 434–441 (2013).
    Google Scholar 

    33.
    Jacobsen, L. B., Chrenková, M., Sunde, P. & Salek, M. Effects of food provisioning and habitat management on spatial behaviour of little owls during the breeding season. Ornis Fenn. 93, 121–129 (2016).
    Google Scholar 

    34.
    Zeller, K. A., Lewsion, R., Fletcher, R. J., Tulbure, M. G. & Jennings, M. K. Understanding the importance of dynamic landscape connectivity. Land (Basel) 9, 303 (2020).
    Google Scholar 

    35.
    Doherty, T. S. & Driscoll, D. A. Coupling movement and landscape ecology for animal conservation in production landscapes. Proc. R. Soc. Lond. B 285, 20172272 (2018).
    Google Scholar 

    36.
    Rohatgi, A. WebPlotDigitizer, version 4.2 (2019); https://automeris.io/WebPlotDigitizer

    37.
    Börger, L. et al. Effects of sampling regime on the mean and variance of home range size estimates. J. Anim. Ecol. 75, 1393–1405 (2006).
    PubMed  Google Scholar 

    38.
    Viechtbauer, W. Conducting meta-analyses in R with the metafor package. J. Stat. Softw. 36, 1–48 (2010).
    Google Scholar 

    39.
    Hedges, L. V., Gurevitch, J. & Curtis, P. S. The meta-analysis of response ratios in experimental ecology. Ecology 80, 1150–1156 (1999).
    Google Scholar 

    40.
    Neumann, W., Ericsson, G. & Dettki, H. Does off-trail backcountry skiing disturb moose? Eur. J. Wildl. Res. 56, 513–518 (2010).
    Google Scholar 

    41.
    Wilman, H. et al. EltonTraits 1.0: species-level foraging attributes of the world’s birds and mammals. Ecology 95, 2027 (2014).
    Google Scholar 

    42.
    Feldman, A., Sabath, N., Pyron, R. A., Mayrose, I. & Meiri, S. Body sizes and diversification rates of lizards, snakes, amphisbaenians and the tuatara. Glob. Ecol. Biogeogr. 25, 187–197 (2016).
    Google Scholar 

    43.
    Oliveira, B. F., São-Pedro, V. A., Santos-Barrera, G., Penone, C. & Costa, G. C. AmphiBIO, a global database for amphibian ecological traits. Sci. Data 4, 170123 (2017).
    PubMed  PubMed Central  Google Scholar 

    44.
    Froese, R. & Pauly, D. (eds) Fishbase (2019); www.fishbase.org

    45.
    Myers, P. et al. The Animal Diversity Web (Univ. Michigan, 2020); https://animaldiversity.org

    46.
    AmphibiaWeb (Univ. California Berkeley, 2020); https://amphibiaweb.org

    47.
    Froese, R., Thorson, J. T. & Reyes, R. B. A Bayesian approach for estimating length–weight relationships in fishes. J. Appl. Ichthyol. 30, 78–85 (2014).
    Google Scholar 

    48.
    Meiri, S. Traits of lizards of the world: variation around a successful evolutionary design. Glob. Ecol. Biogeogr. 27, 1168–1172 (2018).
    Google Scholar 

    49.
    Bürkner, P. C. Advanced Bayesian multilevel modeling with the R package brms. R J. 10, 395–411 (2018).
    Google Scholar 

    50.
    Bürkner, P. C. brms: an R package for Bayesian multilevel models using Stan. J. Stat. Softw. 80, 1–28 (2017).
    Google Scholar 

    51.
    Williams, D. R., Rast, P. & Bürkner, P.-C. Bayesian meta-analysis with weakly informative prior distributions. Preprint at PsyArXiv https://doi.org/10.31234/osf.io/7tbrm (2018).

    52.
    Gelman, A. & Rubin, D. B. Inference from iterative simulation using multiple sequences. Stat. Sci. 7, 457–511 (1992).
    Google Scholar 

    53.
    Egger, M., Davey Smith, G., Schneider, M. & Minder, C. Bias in meta-analysis detected by a simple, graphical test. BMJ 315, 629–634 (1997).
    CAS  PubMed  PubMed Central  Google Scholar 

    54.
    Rosenberg, M. S. The file-drawer problem revisted: a general weighted method for calculating fail-safe numbers in meta-analysis. Evolution 59, 464–468 (2005).
    PubMed  Google Scholar  More