BMC Microbiology | |
Bacteria dialog with Santa Rosalia: Are aggregations of cosmopolitan bacteria mainly explained by habitat filtering or by ecological interactions? | |
Ugo Bastolla2  Javier Tamames1  Alberto Pascual-García2  | |
[1] Centro Nacional de Biotecnologí a (CSIC) c. Darwin 3, campus UAM, Madrid E-28049, Spain;Centro de Biología Molecular Severo Ochoa (CSIC-UAM), c. Nicolás Cabrera 1, campus UAM, Madrid E-28049, Spain | |
关键词: Ecological networks; Ecological null-models; Black queen hypothesis; Bacterial speciation; Syntrophy; Cooperation; Biodiversity; Habitat filtering; Bacterial ecology; | |
Others : 1131231 DOI : 10.1186/s12866-014-0284-5 |
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received in 2014-06-23, accepted in 2014-11-04, 发布年份 2014 | |
【 摘 要 】
Background
Since the landmark Santa Rosalia paper by Hutchinson, niche theory addresses the determinants of biodiversity in terms of both environmental and biological aspects. Disentangling the role of habitat filtering and interactions with other species is critical for understanding microbial ecology. Macroscopic biogeography explores hypothetical ecological interactions through the analysis of species associations. These methods have started to be incorporated into microbial ecology relatively recently, due to the inherent experimental difficulties and the coarse grained nature of the data.
Results
Here we investigate the influence of environmental preferences and ecological interactions in the tendency of bacterial taxa to either aggregate or segregate, using a comprehensive dataset of bacterial taxa observed in a wide variety of environments. We assess significance of taxa associations through a null model that takes into account habitat preferences and the global distribution of taxa across samples. The analysis of these associations reveals a surprisingly large number of significant aggregations between taxa, with a marked community structure and a strong propensity to aggregate for cosmopolitan taxa. Due to the coarse grained nature of our data we cannot conclusively reject the hypothesis that many of these aggregations are due to environmental preferences that the null model fails to reproduce. Nevertheless, some observations are better explained by ecological interactions than by habitat filtering. In particular, most pairs of aggregating taxa co-occur in very different environments, which makes it unlikely that these associations are due to habitat preferences, and many are formed by cosmopolitan taxa without well defined habitat preferences. Moreover, known cooperative interactions are retrieved as aggregating pairs of taxa. As observed in similar studies, we also found that phylogenetically related taxa are much more prone to aggregate than to segregate, an observation that may play a role in bacterial speciation.
Conclusions
We hope that these results stimulate experimental verification of the putative cooperative interactions between cosmopolitan bacteria, and we suggest several groups of aggregated cosmopolitan bacteria that are interesting candidates for such an investigation.
【 授权许可】
2014 Pascual-García et al.; licensee BioMed Central Ltd.
【 预 览 】
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20150301023725300.pdf | 458KB | download | |
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Figure 1. | 22KB | Image | download |
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【 参考文献 】
- [1]Hutchinson GE: Homage to Santa Rosalia or why are there so many kinds of animals? The American Naturalist 1959, 93:145-159.
- [2]McFall-Ngai M, Hadfield MG, Bosch TC, Carey HV, Domazet-LoÅa̧o T, Douglas AE, Dubilier N, Eberl G, Fukami T, Gilbert SF, Hentschel U, King N, Kjelleberg S, Knoll AH, Kremer N, Mazmanian SK, Metcalf JL, Nealson K, Pierce NE, Rawls JF, Reid A, Ruby EG, Rumpho M, Sanders JG, Tautz D, Wernegreen JJ: Animals in a bacterial world, a new imperative for the life sciences. Proc Natl Acad Sci USA 2013, 110:3229-3236.
- [3]Eckburg PB, Bik EM, Bernstein CN, Purdom E, Dethlefsen L, Sargent M, Gill SR, Nelson KE, Relman DA: Diversity of the human intestinal microbial flora. Science 2005, 308:1635-1638.
- [4]Ley RE, Lozupone CA, Hamady M, Knight R, Gordon JI: Worlds within worlds: evolution of the vertebrate gut microbiota. Nat Rev Microbiol 2008, 10:776-788.
- [5]Qin J, Li R, Raes J, Arumugam M, Burgdorf KS, Manichanh C, Nielsen T, Pons N, Levenez F, Yamada T, Mende DR, Li J, Xu J, Li S, Li D, Cao J, Wang B, Liang H, Zheng H, Xie Y, Tap J, Lepage P, Bertalan M, Batto JM, Hansen T, Le Paslier D, Linneberg A, Nielsen HB, Pelletier E, Renault P, et al.: Human gut microbial gene catalogue established by metagenomic sequencing. Nature 2010, 464:59-65.
- [6]The Human MicrobiomeProjectConsortium: Structure, function and diversity of the healthy human microbiome. Nature 2012, 486:207-214.
- [7]Horner-Devine MC, Carney KM, Bohannan BJM: An ecological perspective on bacterial biodiversity. Proc R Soc Lond B 2003, 271:113-122.
- [8]Horner-Devine MC, Lage M, Hughes JB, Bohannan BJM: A taxa-area relationship for bacteria. Nature 2004, 432:750-753.
- [9]Green J, Bohannan BJM: Spatial scaling of microbial biodiversity. Trends Ecol Evol 2006, 21:501-507.
- [10]Rocap G, Larimer FW, Lamerdin J, Malfatti S, Chain P, Ahlgren NA, Arellano A, Coleman M, Hauser L, Hess WR, Johnson ZI, Land M, Lindell D, Post AF, Regala W, Shah M, Shaw SL, Steglich C, Sullivan MB, Ting CS, Tolonen A, Webb EA, Zinser ER, Chisholm SW: Genome divergence in two prochlorococcus ecotypes reflects oceanic niche differentiation. Nature 2003, 424:1042-1047.
- [11]Hopkinson CS, Sogin ML, Hobbie JE, Crump BC: Microbial biogeography along an estuarine salinity gradient: combined influences of bacterial growth and residence time. Appl Environ Microbiol 2004, 70:1494-1505.
- [12]Ramette A, Tiedje JM: Biogeography: An emerging cornerstone for understanding prokaryotic diversity, ecology and evolution. Microb Ecol 2006, 53:197-207.
- [13]Martiny JB, Bohannan BJ, Brown JH, Colwell RK, Fuhrman JA, Green JL, Horner-Devine MC, Kane M, Krumins JA, Kuske CR, Morin PJ, Naeem S, OvreÃěs L, Reysenbach AL, Smith VH, Staley JT: Microbial biogeography: putting microorganisms on the map. Nat Rev Microbiol 2006, 4:102-112.
- [14]Vellend M: Conceptual synthesis in community ecology. Q Rev Biol 2010, 85:183-206.
- [15]Freilich S, Kreimer A, Meilijson I, Gophna U, Sharan R, Ruppin E: The large-scale organization of the bacterial network of ecological co-occurrence interactions. Nucl Ac Res 2010, 38:3857-68.
- [16]Horner-Devine MC, Silver JM, Leibold MA, Bohannan BJ, Colwell RK, Fuhrman JA, Green JL, Kuske CR, Martiny JB, Muyzer G, OvreÃěs L, Reysenbach AL, Smith VH: A comparison of taxon co-occurrence patterns for macro- and microorganisms. Ecology 2007, 88:1345-1353.
- [17]Chaffron S, Rehrauer H, Pernthaler J, von Mering C: A global network of coexisting microbes from environmental and whole-genome sequence data. Genome Res 2010, 20:947-959.
- [18]Arumugam M, Raes J, Pelletier E, Le Paslier D, Yamada T, Mende DR, Fernandes GR, Tap J, Bruls T, Batto JM, Bertalan M, Borruel N, Casellas F, Fernandez L, Gautier L, Hansen T, Hattori M, Hayashi T, Kleerebezem M, Kurokawa K, Leclerc M, Levenez F, Manichanh C, Nielsen HB, Nielsen T, Pons N, Poulain J, Qin J, Sicheritz-Ponten T, Tims S, et al.: Enteroptypes of the human gut microbiome. Nature 2011, 473:174-180.
- [19]Barberán A, Bates ST, Casamayor EO, Fierer N: Using network analysis to explore co-occurrence patterns in soil microbial communities. ISME J 2012, 6:343-51.
- [20]Deng Y, Jiang YH, Yang Y, He Z, Luo F, Zhou J: Molecular ecological network analyses. BMC Bioinformatics 2012, 13:11. BioMed Central Full Text
- [21]Gilbert JA, Steele JA, Caporaso JG, SteinbrÃijck L, Reeder J, Temperton B, Huse S, McHardy AC, Knight R, Joint I, Somerfield P, Fuhrman JA, Field D: Defining seasonal marine microbial community dynamics. ISME J 2012, 6:298-308.
- [22]Larsen PE, Field D, Gilbert JA: Predicting bacterial community assemblages using an artificial neural network apprach. Nat Methods 2012, 9:621-625.
- [23]Lozupone C, Faust K, Raes J, Faith JJ, Frank DN, Zaneveld J, Gordon JI, Knight R: Identifying genomic and metabolic features that can underlie early successional and opportunistic lifestyles of human gut symbionts. Genome Res 2012, 22:1974-1984.
- [24]Faust K, Sathirapongsasuti JF, Izard J, Segata N, Gevers D, Raes J, Huttenhower C: Microbial co-occurrence relationships in the human microbiome. PLoS Comp Biol 2012, 8:e1002606.
- [25]Faust K, Raes J: Microbial interactions: from networks to models. Nat Rev Microbiol 2012, 10:538-550.
- [26]Tamames J, Abellán JJ, Pignatelli M, Camacho A, Moya A: Environmental distribution of prokaryotic taxa. BMC Microbiol 2010, 10:85. BioMed Central Full Text
- [27]Navarro-Alberto JA, Manly BFJ: Null model analyses of presence-absence matrices need a definition of independence. Popul Ecol 2009, 51:505-512.
- [28]Freilich S, Zarecki R, Eilam O, Segal ES, Henry CS, Kupiec M, Gophna U, Sharan R, Ruppin E: Competitive and cooperative metabolic interactions in bacterial communities. Nat Commun 2011, 2:589.
- [29]Bascompte J, Jordano P, Melián CJ, Olesen JM: The nested assembly of plantanimal mutualistic networks. Proc Natl Acad Sci USA 2003, 100:9383-9387.
- [30]Schink B, Stams AJM: Syntrophism among prokaryotes. In The Prokaryotes . Edited by Dworkin M. Springer, vol. 2. New York; 2006:309-335.
- [31]Boyle KE, Heilmann S, van Ditmarsch D, Xavier JB: Exploiting social evolution in biofilms. Curr Opin Microbiol 2013, 16(2):207-212.
- [32]Dowd SE, Sun Y, Secor PR, Rhoads DD, Wolcott BM, James GA, Wolcott RD: Survey of bacterial diversity in chronic wounds using pyrosequencing, DGGE, and full ribosome shotgun sequencing. BMC Microbiol 2008, 8:43. BioMed Central Full Text
- [33]Ramirez-Puebla ST, Servin-Garcidueñas LE, Jimenez-Marin B, Bolaños LM, Rosenblueth M, Martinez J, Rogel MA, Ormeño-Orrillo E, Martinez-Romero E: Gut and root microbiota commonalities. Appl Environ Microbiol 2013, 79:2-9.
- [34]Stams AJ, Plugge CM, de Bok FA, van Houten BH, Lens P, Dijkman H, Weijma J: Metabolic interactions in methanogenic and sulfate-reducing bioreactors. Water Sci Technol 2005, 52:13-20.
- [35]Tatton MJ, Archer DB, Powell GE, Parker ML: Methanogenesis from ethanol by defined mixed continuous cultures. Appl Environ Microbiol 1989, 55:440-445.
- [36]Lerm S, Kleyböcker A, Miethling-Graff R, Alawi M, Kasina M, Liebrich M, Würdemann H: Archaeal community composition affects the function of anaerobic co-digesters in response to organic overload. Waste Manag 2012, 32:389-399.
- [37]Hansen SK, Rainey PB, Haagensen JA, Molin S: Evolution of species interactions in a biofilm community. Nature 2007, 445:533-536.
- [38]Siripong S, Rittmann BE: Diversity study of nitrifying bacteria in full-scale municipal wastewater treatment plants. Water Res 2007, 41:1110-1120.
- [39]González-Toril E, Llobet-Brossa E, Casamayor EO, Amann R, Amils R: Microbial ecology of an extreme acidic environment, the Tinto River. Appl Environ Microbiol 2003, 69:48534865.
- [40]Santofimia E, Gonzàlez-Toril E, López-Pamo E, Gomariz M, Amils R, Aguilera A: Microbial diversity and its relationship to physicochemical characteristics of the water in two extreme acidic pit lakes from the iberian pyrite belt (SW Spain). PLoS ONE 2013, 8(6):e66746.
- [41]Katsuyama C, Nakaoka S, Takeuchi Y, Tago K, Hayatsu M, Kato K: Complementary cooperation between two syntrophic bacteria in pesticide degradation. J Theor Biol 2009, 256:644-654.
- [42]Eberl L, Tümmler B: Pseudomonas aeruginosa and Burkholderia cepacia in cystic fibrosis: genome evolution, interactions and adaptation. Int J Med Microbiol 2004, 294:123-131.
- [43]Rivas R, Velázquez E, Willems A, Vizcaíno N, Subba-Rao NS, Mateos PF, Gillis M, Dazzo FB, Martínez-Molina E: A new species of Devosia that forms a unique nitrogen-fixing root-nodule symbiosis with the aquatic legume Neptunia natans (L.f.) druce. Appl Environ Microbiol 2002, 68:5217-5222.
- [44]Douglas AE, Smith DC: Are endosymbioses mutualistic? Trends Ecol Evol 1989, 4:350-352.
- [45]Blondel VD, Guillaume JL, Lambiotte R, Lefebvre E: Fast unfolding of communities in large networks. J Stat Mech Theor Exp 2008, 10:1000.
- [46][www.aaai.org] webcite Bastian M, Heymann S, Jacomy M: Gephi: an open source software for exploring and manipulating networks. In International AAAI Conference on Weblogs and Social Media; 2009. Association for the Advancement of Artificial Intelligence ().
- [47][http://vlado.fmf.uni-lj.si/pub/networks/pajek/] webcite Batagelj V, Mrvar A: Pajek: A Program for Large Network Analysis. Home page: .
- [48]Vallès Y, Artacho A, Pascual-García A, Ferrús ML, Gosalbes MJ, Abellán JJ, Francino MP: Successional patterns of community assembly and functional ecology during gut microbiota development in an infant birth cohort. PLoS Genetics 2014, 10:e1004406. Aceptado en PloS Genetics
- [49]Lozupone CA, Stombaugh JI, Gordon JI, Jansson JK, Knight R: Diversity, stability and resilience of the human gut microbiota. Nature 2012, 489:220-230.
- [50]Curtis TP, Sloan WT, Scannell JW: Estimating prokaryotic diversity and its limits. Proc Natl Acad Sci USA 2002, 99:10494-10499.
- [51]Dykhuizen DE: Santa Rosalia revisited: Why are there so many species of bacteria? Antonie Leeuwenhaek 1998, 73:25-33.
- [52]Schloss PD, Handelsman J: Status of the microbial census. Microbiol Mol Biol Rev 2004, 68:686-691.
- [53]Mora C, Tittensor DP, Adl S, Simpson AGB, Worm B: How Many Species Are There on Earth and in the Ocean? PLoS Biol 2011, 9(8):e1001127.
- [54]Staley JT: The bacterial species dilemma and the genomic-phylogenetic species concept. Philos Trans R Soc Lond B Biol Sci 2006, 361:1899-1909.
- [55]Cohan FM: What are bacterial species? Annu Rev Microbiol 2002, 56:457-487.
- [56]Philippot L, Andersson SG, Battin TJ, Prosser JI, Schimel JP, Whitman WB, Hallin S: The ecological coherence of high bacterial taxonomic ranks. Nat Rev Microbiol 2010, 8:523-529.
- [57]Bastolla U, Fortuna MA, Pascual-García A, Ferrera A, Luque B, Bascompte J: The architecture of mutualistic networks minimizes competition and increases biodiversity. Nature 2009, 458:1018-1020.
- [58]Koeppel AF, Wu M: Species matter: the role of competition in the assembly of congeneric bacteria. ISME J 2014, 8:531-540.
- [59]Stone L, Roberts A: The checkerboard score and species distribution. Oecologia 1990, 85:74-79.
- [60]Gotelli NJ, Ulrich W: The empirical bayes approach as a tool to identify non-random species associations. Oecologia 2010, 162:463-477.
- [61]Levy R, Borenstein E: Metabolic modeling of species interaction in the human microbiome elucidates community-level assembly rules. Proc Natl Acad Sci USA 2013, 110:12804-12809.
- [62]Mee MT, Collins JJ, Church GM, Wang HH: Syntrophic exchange in synthetic microbial communities. Proc Natl Acad Sci USA 2014, 111:E2149-E2156.
- [63]Klitgord N, Segré D: Environments that induce synthetic microbial ecosystems. PLoS Comp Biol 2010, 6:e1001002.
- [64]Foster KR, Bell T: Competition, not cooperation, dominates interactions among culturable microbial species. Curr Biol 2012, 22:1845-1850.
- [65]Carlson CA, del Giorgio PA, Herndl GJ: Microbes and the dissipation of energy and respiration: from cells to ecosystems. Oceanography 2007, 20(2):89100.
- [66]Lawrence D, Fiegna F, Behrends V, Bundy JG, Phillimore AB, Bell T, Barraclough TG: Species interactions alter evolutionary responses to a novel environment. PLoS Biol 2012, 10:e1001330.
- [67]Cordero OX, Wildschutte H, Kirkup B, Proehl S, Ngo L, Hussain F, Le Roux F, Mincer T, Polz MF: Ecological populations of bacteria act as socially cohesive units of antibiotic production and resistance. Science 2012, 337:1228-1231.
- [68]Velicer GJ, Yu YN: Evolution of novel cooperative swarming in the bacterium Myxococcus xanthus. Nature 2003, 425:75-78.
- [69]Harcombe W: Novel cooperation experimentally evolved between species. Evolution 2010, 64:2166-2172.
- [70]Hosoda K, Suzuki S, Yamauchi Y, Shiroguchi Y, Kashiwagi A, Ono N, Mori K, Yomo T: Cooperative adaptation to establishment of a synthetic bacterial mutualism. PLoS ONE 2011, 6(2):e17105.
- [71]Waite AJ, Shou W: Adaptation to a new environment allows cooperators to purge cheaters stochastically. Proc Natl Acad Sci U S A 2012, 109:19079-19086.
- [72]Ferriere R, Bronstein JL, Rinaldi S, Law R, Gauduchon M: Cheating and the evolutionary stability of mutualisms. Proc R Soc London. Series B: Biol Sci 2002, 269(1493):773-780.
- [73]Morris JJ, Lenski RE, Zinser ER: The Black Queen Hypothesis: evolution of dependencies through adaptive gene loss. MBio 2012, 3(2):e00036-12. doi:10.1128/mBio.00036-12.
- [74]Sachs JL, Hollowell AC: The origins of cooperative bacterial communities. MBio 2012, 3(3):e00099-12. doi:10.1128/mBio.00099-12.
- [75]Kettler GC, Martiny AC, Huang K, Zucker J, Coleman ML, Rodrigue S, Chen F, Lapidus A, Ferriera S, Johnson J, Steglich C, Church GM, Richardson P, Chisholm SW: Patterns and implications of gene gain and loss in the evolution of Prochlorococcus. PLoS Genet 2007, 3:e231.
- [76]Gilpin ME, Diamond JM: Factors contributing to non-randomness in species co-occurrences on islands. Oecologia 1982, 52:75-84.