Where less may be more: how the rare biosphere pulls ecosystems strings

ISME Journal - Tập 11 Số 4 - Trang 853-862 - 2017
Alexandre Jousset1, Christina Bienhold2,3, Antonis Chatzinotas4,5, Laure Gallien6,7, Angélique Gobet8, Viola Kurm9, Kirsten Küsel4,4, Matthias C. Rillig10,11, Damian Rivett12, Joana Falcão Salles13, Marcel G. A. van der Heijden14,15,16, Noha H. Youssef17, Xiaowei Zhang18, Zhong Wei19, W. H. Gera Hol9
1Utrecht University, Department of Biology, Institute of Environmental Biology, Ecology and Biodiversity Group , Utrecht, The Netherlands
2Alfred Wegener Institute Helmholtz Centre for Polar and Marine Research, Bremerhaven, Germany
3Max Planck Institute for Marine Microbiology, Bremen, Germany
4German Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-Leipzig, Leipzig, Germany
5Helmholtz Centre for Environmental Research UFZ, Leipzig, Germany
6Center for Invasion Biology, Department of Botany & Zoology, Stellenbosch University , Matieland, South Africa
7Swiss Federal Institute for Forest, Snow and Landscape Research WSL, Birmensdorf, Switzerland
8Sorbonne Universités, UPMC Université Paris 06, CNRS, UMR 8227, Integrative Biology of Marine Models, Station Biologique de Roscoff , F-29688, Roscoff Cedex, France
9Netherlands Institute of Ecology, Department of Terrestrial Ecology, Wageningen, The Netherlands
10Berlin-Brandenburg Institute of Advanced Biodiversity Research (BBIB), Berlin, Germany
11Freie Universtät Berlin, Institute of Biology , Berlin, Germany
12Imperial College London, Department of Life Sciences, Silwood Park Campus , Ascot, UK
13Groningen Institute for Evolutionary Life Sciences, University of Groningen, Groningen, The Netherlands
14Institute of Evolutionary Biology and Environmental Studies, University of Zürich, Zürich, Switzerland
15Plant-Soil Interactions, Institute for Sustainability Sciences, Agroscope, Zürich, Switzerland
16Plant-Microbe Interactions, Institute of Environmental Biology, Faculty of Science, Utrecht University, Utrecht, The Netherlands
17Oklahoma State University, Department of Microbiology and Molecular Genetics , Stillwater, OK, USA
18State Key Laboratory of Pollution Control & Resource Reuse, School of the Environment, Nanjing University, Nanjing, China
19Nanjing Agricultural University, Nanjing, China

Tóm tắt

Abstract Rare species are increasingly recognized as crucial, yet vulnerable components of Earth’s ecosystems. This is also true for microbial communities, which are typically composed of a high number of relatively rare species. Recent studies have demonstrated that rare species can have an over-proportional role in biogeochemical cycles and may be a hidden driver of microbiome function. In this review, we provide an ecological overview of the rare microbial biosphere, including causes of rarity and the impacts of rare species on ecosystem functioning. We discuss how rare species can have a preponderant role for local biodiversity and species turnover with rarity potentially bound to phylogenetically conserved features. Rare microbes may therefore be overlooked keystone species regulating the functioning of host-associated, terrestrial and aquatic environments. We conclude this review with recommendations to guide scientists interested in investigating this rapidly emerging research area.

Từ khóa


Tài liệu tham khảo

Aanderud, 2015, Resuscitation of the rare biosphere contributes to pulses of ecosystem activity, Front Microbiol, 6, 24, 10.3389/fmicb.2015.00024

Ai, 2013, Migration and niche partitioning simultaneously increase species richness and rarity, Ecol Model, 258, 33, 10.1016/j.ecolmodel.2013.03.001

Allan, 2011, More diverse plant communities have higher functioning over time due to turnover in complementary dominant species, Proc Natl Acad Sci USA, 108, 17034, 10.1073/pnas.1104015108

Barberán, 2014, Why are some microbes more ubiquitous than others? Predicting the habitat breadth of soil bacteria, Ecol Lett, 17, 794, 10.1111/ele.12282

Baumann, 2013, Soil microbial diversity affects soil organic matter decomposition in a silty grassland soil, Biochemistry, 114, 201

Bittinger, 2014, Improved characterization of medically relevant fungi in the human respiratory tract using next-generation sequencing, Genome Biol, 15, 487, 10.1186/s13059-014-0487-y

Bodelier, 2013, Microbial minorities modulate methane consumption through niche partitioning, ISME J, 7, 2214, 10.1038/ismej.2013.99

Brown, 2015, Unusual biology across a group comprising more than 15% of domain bacteria, Nature, 523, 208, 10.1038/nature14486

Campbell, 2011, Activity of abundant and rare bacteria in a coastal ocean, Proc Natl Acad Sci USA, 108, 12776, 10.1073/pnas.1101405108

Chambers, 2016, Effects of salinity and inundation on microbial community structure and function in a mangrove peat soil, Wetlands, 36, 361, 10.1007/s13157-016-0745-8

Chen, 2010, When metagenomics meets stable-isotope probing: progress and perspectives, Trends Microbiol, 18, 157, 10.1016/j.tim.2010.02.002

Debroas, 2015, Evidence for an active rare biosphere within freshwater protists community, Mol Ecol, 24, 1236, 10.1111/mec.13116

Delgado-Baquerizo, 2016, Lack of functional redundancy in the relationship between microbial diversity and ecosystem functioning, J Ecol, 104, 936, 10.1111/1365-2745.12585

Dell’Anno, 2012, High bacterial biodiversity increases degradation performance of hydrocarbons during bioremediation of contaminated harbor marine sediments, Environ Pollut, 167, 85, 10.1016/j.envpol.2012.03.043

Dimitriu, 2010, An evaluation of the functional significance of peat microorganisms using a reciprocal transplant approach, Soil Biol Biochem, 42, 65, 10.1016/j.soilbio.2009.10.001

Falkowski, 2008, The microbial engines that drive Earth’s biogeochemical cycles, Science, 320, 1034, 10.1126/science.1153213

Fetzer, 2015, The extent of functional redundancy changes as species’ roles shift in different environments, Proc Natl Acad Sci USA, 112, 14888, 10.1073/pnas.1505587112

Franklin, 2001, Impact of dilution on microbial community structure and functional potential: comparison of numerical simulations and batch culture experiments, Appl Environ Microbiol, 67, 702, 10.1128/AEM.67.2.702-712.2001

Franklin, 2006, Structural and functional responses of a sewage microbial community to dilution-induced reductions in diversity, Microb Ecol, 52, 280, 10.1007/s00248-006-9033-0

Freilich, 2011, Competitive and cooperative metabolic interactions in bacterial communities, Nat Commun, 2, 589, 10.1038/ncomms1597

Fuentes, 2014, Bioremediation of petroleum hydrocarbons: catabolic genes, microbial communities, and applications, Appl Microbiol Biotechnol, 98, 4781, 10.1007/s00253-014-5684-9

Fukami, 2003, Productivity-biodiversity relationships depend on the history of community assembly, Nature, 424, 423, 10.1038/nature01785

Gagic, 2015, Improving the genetic representation of rare taxa within complex microbial communities using DNA normalization methods, Mol Ecol Res, 15, 464, 10.1111/1755-0998.12321

Garbeva, 2011, Transcriptional and antagonistic responses of Pseudomonas fluorescens Pf0-1 to phylogenetically different bacterial competitors, ISME J, 5, 973, 10.1038/ismej.2010.196

García-Fernández, 2004, Streamlined regulation and gene loss as adaptive mechanisms in Prochlorococcus for optimized nitrogen utilization in oligotrophic environments, Microbiol Mol Biol Rev, 68, 630, 10.1128/MMBR.68.4.630-638.2004

Garland, 1999, Survival of human-associated bacteria in prototype advanced life support systems, SAE Techical paper 1999-01-2061, American Society of Automotive Engineers, 10.4271/1999-01-2061

Gaston, 2008, Biodiversity and extinction: the importance of being common, Prog Phys Geogr, 32, 73, 10.1177/0309133308089499

Giebler, 2013, Alkane-degrading bacteria at the soil-litter interface: comparing isolates with T-RFLP-based community profiles, FEMS Microbiol Ecol, 86, 45, 10.1111/1574-6941.12097

Gobet, 2012, Diversity and dynamics of rare and of resident bacterial populations in coastal sands, ISME J, 6, 542, 10.1038/ismej.2011.132

Griffiths, 2001, An examination of the biodiversity-ecosystem function relationship in arable soil microbial communities, Soil Biol Biochem, 33, 1713, 10.1016/S0038-0717(01)00094-3

Griffiths, 2004, The relationship between microbial community structure and functional stability, tested experimentally in an upland pasture soil, Microb Ecol, 47, 104, 10.1007/s00248-002-2043-7

Gudelj, 2010, An integrative approach to understanding microbial diversity: from intracellular mechanisms to community structure, Ecol Lett, 13, 1073, 10.1111/j.1461-0248.2010.01507.x

Guss, 2011, Phylogenetic and metabolic diversity of bacteria associated with cystic fibrosis, ISME J, 5, 20, 10.1038/ismej.2010.88

Hajishengallis, 2011, Low-abundance biofilm species orchestrates inflammatory periodontal disease through the commensal microbiota and complement, Cell Host Microbe, 10, 497, 10.1016/j.chom.2011.10.006

Haruta, 2009, Intertwined interspecies relationships: approaches to untangle the microbial network, Environ Microbiol, 11, 2963, 10.1111/j.1462-2920.2009.01956.x

Hausmann, 2016, Consortia of low-abundance bacteria drive sulfate reduction-dependent degradation of fermentation products in peat soil microcosms, ISME J, 10, 2365, 10.1038/ismej.2016.42

Hedlund, 2014, Impact of single-cell genomics and metagenomics on the emerging view of extremophile ‘microbial dark matter’, Extremophiles, 18, 865, 10.1007/s00792-014-0664-7

Helliwell, 2013, Widespread decay of vitamin-related pathways: coincidence or consequence?, Trends Genet, 29, 469, 10.1016/j.tig.2013.03.003

Hernandez-Raquet, 2013, Impact of microbial diversity depletion on xenobiotic degradation by sewage-activated sludge, Environ Microbiol Rep, 5, 588, 10.1111/1758-2229.12053

Herrera, 1989, Pollinator abundance, morphology, and flower visitation rate - analysis of the quantity component in a plant-pollinator system, Oecologia, 80, 241, 10.1007/BF00380158

Hol, 2010, Reduction of rare soil microbes modifies plant-herbivores interactions, Ecol Lett, 13, 292, 10.1111/j.1461-0248.2009.01424.x

Hol, 2015, Context dependency and saturating effects of loss of rare soil microbes on plant productivity, Front Plant Sci, 6, 485, 10.3389/fpls.2015.00485

Hol, 2015, Non-random species loss in bacterial communities reduces antifungal volatile production, Ecology, 96, 2042, 10.1890/14-2359.1

Hua, 2015, Ecological roles of dominant and rare prokaryotes in acid mine drainage revealed by metagenomics and metatranscriptomics, ISME J, 9, 1280, 10.1038/ismej.2014.212

Jimenez, 2014, Novel multispecies microbial consortia involved in lignocellulose and 5-hydroxymethylfurfural bioconversion, Appl Microbiol Biotechnol, 98, 2789, 10.1007/s00253-013-5253-7

Jousset, 2009, Predators promote defence of rhizosphere bacterial populations by selective feeding on non-toxic cheaters, ISME J, 3, 666, 10.1038/ismej.2009.26

Jousset, 2013, Evolutionary history predicts the stability of cooperation in microbial communities, Nat Commun, 4, 2573, 10.1038/ncomms3573

Kummerli, 2010, Molecular and regulatory properties of a public good shape the evolution of cooperation, Proc Natl Acad Sci USA, 107, 18921, 10.1073/pnas.1011154107

Leitão, 2016, Rare species contribute disproportionately to the functional structure of species assemblages, Proc R Soc Lond Ser B Biol Sci, 283, 20160084, 10.1098/rspb.2016.0084

Li, 2008, Simultaneous analysis of microbial identity and function using NanoSIMS, Environ Microbiol, 10, 580, 10.1111/j.1462-2920.2007.01478.x

Locey, 2016, Scaling laws predict global microbial diversity, Proc Natl Acad Sci USA, 113, 5970, 10.1073/pnas.1521291113

Low-Décarie, 2015, Community rescue in experimental metacommunities, Proc Natl Acad Sci USA, 112, 14307, 10.1073/pnas.1513125112

Loy, 2010, Geomicrobiology: Molecular and Environmental Perspective, 127, 10.1007/978-90-481-9204-5_6

Lynch, 2015, Ecology and exploration of the rare biosphere, Nat Rev Microbiol, 13, 217, 10.1038/nrmicro3400

Lyons, 2005, Rare species and ecosystem functioning, Conserv Biol, 19, 1019, 10.1111/j.1523-1739.2005.00106.x

Mallon, 2015, Resource pulses can alleviate the biodiversity-invasion relationship in soil microbial communities, Ecology, 96, 915, 10.1890/14-1001.1

Matos, 2005, Effects of microbial community diversity on the survival of Pseudomonas aeruginosa in the wheat rhizosphere, Microb Ecol, 49, 257, 10.1007/s00248-004-0179-3

McMurdie, 2014, Waste not, want not: why rarefying microbiome data is inadmissible, PLoS Comp Biol, 10, e1003531, 10.1371/journal.pcbi.1003531

Mee, 2014, Syntrophic exchange in synthetic microbial communities, Proc Natl Acad Sci USA, 111, 2149, 10.1073/pnas.1405641111

Meyer, 2007, The effects of competition and predation on diversification in a model adaptive radiation, Nature, 446, 432, 10.1038/nature05599

Mouillot, 2013, Rare species support vulnerable functions in high diversity ecosystems, PLoS Biol, 11, 11, 10.1371/journal.pbio.1001569

Musat, 2008, A single-cell view on the ecophysiology of anaerobic phototrophic bacteria, Proc Natl Acad Sci USA, 105, 17861, 10.1073/pnas.0809329105

Narisawa, 2008, Coexistence of antibiotic-producing and antibiotic-sensitive bacteria in biofilms is mediated by resistant bacteria, Appl Environ Microbiol, 74, 3887, 10.1128/AEM.02497-07

Nemergut, 2011, Global patterns in the biogeography of bacterial taxa, Environ Microbiol, 13, 135, 10.1111/j.1462-2920.2010.02315.x

Nipperess, 2013, The mean and variance of phylogenetic diversity under rarefaction, Methods Ecol Evol, 4, 566, 10.1111/2041-210X.12042

Nuccio, 2016, Climate and edaphic controllers influence rhizosphere community assembly for a wild annual grass, Ecology, 97, 1307, 10.1890/15-0882.1

Panaud, 2016, Horizontal transfers of transposable elements in eukaryotes: the flying genes, C R Biol, 339, 296, 10.1016/j.crvi.2016.04.013

Pedrós-Alió, 2007, Dipping into the rare biosphere, Science, 315, 192, 10.1126/science.1135933

Pester, 2010, A ‘rare biosphere’ microorganism contributes to sulfate reduction in a peatland, ISME J, 4, 1591, 10.1038/ismej.2010.75

Peter, 2011, Function-specific response to depletion of microbial diversity, ISME J, 5, 351, 10.1038/ismej.2010.119

Philippot, 2013, Loss in microbial diversity affects nitrogen cycling in soil, ISME J, 7, 1609, 10.1038/ismej.2013.34

Podar, 2007, Targeted access to the genomes of low-abundance organisms in complex microbial communities, Appl Environ Microbiol, 73, 3205, 10.1128/AEM.02985-06

Portillo, 2013, Cell size distributions of soil bacterial and archaeal taxa, Appl Environ Microbiol, 79, 7610, 10.1128/AEM.02710-13

Rabinowitz, 1981, The Biological Aspects of Rare Plant Conservation, 205

Reid, 2011, The Rare Biosphere, 1

Rodrigues, 2013, Conversion of the Amazon rainforest to agriculture results in biotic homogenization of soil bacterial communities, Proc Natl Acad Sci USA, 110, 988, 10.1073/pnas.1220608110

Rodriguez-Valera, 2009, Explaining microbial population genomics through phage predation, Nat Rev Microbiol, 7, 828, 10.1038/nrmicro2235

Rousk, 2009, Contrasting soil pH effects on fungal and bacterial growth suggest functional redundancy in carbon mineralization, Appl Environ Microbiol, 75, 1589, 10.1128/AEM.02775-08

Russell, 2014, Nature’s microbiome: introduction, Mol Ecol, 23, 1225, 10.1111/mec.12676

Salonius, 1981, Metabolic capabilities of forest soil microbial-populations with reduced species-diversity, Soil Biol Biochem, 13, 1, 10.1016/0038-0717(81)90094-8

Sanchez, 2004, A previously unexposed forest soil microbial community degrades high levels of the pollutant 2,4,6-trichlorophenol, Appl Environ Microbiol, 70, 7567, 10.1128/AEM.70.12.7567-7570.2004

Schadt, 2015, Comment on “Global diversity and geography of soil fungi”, Science, 348, 1438, 10.1126/science.aaa4269

Schluter, 2015, Adhesion as a weapon in microbial competition, ISME J, 9, 139, 10.1038/ismej.2014.174

Shade, 2014, Conditionally rare taxa disproportionately contribute to temporal changes in microbial diversity, Mbio, 5, e01371, 10.1128/mBio.01371-14

Sogin, 2006, Microbial diversity in the deep sea and the underexplored “rare biosphere”, Proc Natl Acad Sci USA, 103, 12115, 10.1073/pnas.0605127103

Soliveres, 2016, Locally rare species influence grassland ecosystem multifunctionality, Philos Trans R Soc Lond Ser B Biol Sci, 371, 20150269, 10.1098/rstb.2015.0269

Stecher, 2013, Colonization resistance and microbial ecophysiology: using gnotobiotic mouse models and single-cell technology to explore the intestinal jungle, FEMS Microbiol Rev, 37, 793, 10.1111/1574-6976.12024

Steger, 2011, Microorganisms with novel dissimilatory (bi)sulfite reductase genes are widespread and part of the core microbiota in low-sulfate peatlands, Appl Environ Microbiol, 77, 1231, 10.1128/AEM.01352-10

Tardy, 2014, Stability of soil microbial structure and activity depends on microbial diversity, Environ Microbiol Rep, 6, 173, 10.1111/1758-2229.12126

Tedersoo, 2014, Global diversity and geography of soil fungi, Science, 346, 1256688, 10.1126/science.1256688

Van der Gast, 2011, Partitioning core and satellite taxa from within cystic fibrosis lung bacterial communities, ISME J, 5, 780, 10.1038/ismej.2010.175

Van Elsas, 2012, Microbial diversity determines the invasion of soil by a bacterial pathogen, Proc Natl Acad Sci USA, 109, 1159, 10.1073/pnas.1109326109

Vivant, 2013, Microbial diversity and structure are drivers of the biological barrier effect against Listeria monocytogenes in soil, Plos One, 8, e76991, 10.1371/journal.pone.0076991

Winter, 2010, Trade-offs between competition and defense specialists among unicellular planktonic organisms: the killing the winner hypothesis revisited, Microbiol Mol Biol Rev, 74, 42, 10.1128/MMBR.00034-09

Yachi, 1999, Biodiversity and ecosystem productivity in a fluctuating environment: The insurance hypothesis, Proc Natl Acad Sci USA, 96, 1463, 10.1073/pnas.96.4.1463

Yan, 2015, Revisiting the dilution procedure used to manipulate microbial biodiversity in terrestrial systems, Appl Environ Microbiol, 81, 4246, 10.1128/AEM.00958-15

Yenni, 2012, Strong self-limitation promotes the persistence of rare species, Ecology, 93, 456, 10.1890/11-1087.1

Youssef, 2015, Assessing the global phylum level diversity within the bacterial domain: a review, J Adv Res, 6, 269, 10.1016/j.jare.2014.10.005

Zhang, 2009, Quantifying the relative importance of niches and neutrality for coexistence in a model microbial system, Funct Ecol, 23, 1139, 10.1111/j.1365-2435.2009.01579.x