Diversity, structure and convergent evolution of the global sponge microbiome

Nature Communications

Volumn 7, Issue , 2016, Pages

  Thomas, Torsten ^a   Moitinho Silva, Lucas ^a   Lurgi, Miguel ^b   Björk, Johannes R ^c,d   Easson, Cole ^e   Astudillo García, Carmen ^f   Olson, Julie B ^g   Erwin, Patrick M ^h   López Legentil, Susanna ^h   Luter, Heidi ⁱ   Chaves Fonnegra, Andia ^j   Costa, Rodrigo ^k   Schupp, Peter J ^l   Steindler, Laura ^m   Erpenbeck, Dirk ⁿ   Gilbert, Jack ^o,p   Knight, Rob ^q   Ackermann, Gail ^q   Victor Lopez, Jose ^j   Taylor, Michael W ^f   Thacker, Robert W ^r   Montoya, Jose M ^c   Hentschel, Ute ^s   Webster, Nicole S ^t   more..

^a UNIVERSITY OF NEW SOUTH WALES   (Australia)

^b UNIVERSITY OF ADELAIDE   (Australia)

^c CNRS   (France)

^d INSTITUT DE CIÈNCIES DEL MAR   (Spain)

^e UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^f UNIVERSITY OF AUCKLAND   (New Zealand)

^g UNIVERSITY OF ALABAMA   (United States)

^h UNIVERSITY OF NORTH CAROLINA WILMINGTON   (United States)

ⁱ CHARLES DARWIN UNIVERSITY   (Australia)

^j NOVA SOUTHEASTERN UNIVERSITY   (United States)

^k UNIVERSITY OF ALGARVE   (Portugal)

^l UNIVERSITY OF OLDENBURG   (Germany)

^m UNIVERSITY OF HAIFA   (Israel)

ⁿ UNIVERSITY OF MUNICH   (Germany)

^o UNIVERSITY OF CHICAGO   (United States)

^p ARGONNE NATIONAL LABORATORY   (United States)

^q UNIVERSITY OF CALIFORNIA   (United States)

^r STONY BROOK UNIVERSITY   (United States)

^s GEOMAR HELMHOLTZ CENTRE FOR OCEAN RESEARCH KIEL   (Germany)

^t AUSTRALIAN INSTITUTE OF MARINE SCIENCE   (Australia)

more..

Author keywords

[No Author keywords available]

Indexed keywords

HOST FACTOR; RNA 16S; SEA WATER;

COMMUNITY COMPOSITION; COMMUNITY ORGANIZATION; COMMUNITY STRUCTURE; CONVERGENT EVOLUTION; METAZOAN; PHYLOGENETICS; PHYLOGENY; SPECIES DIVERSITY; SPONGE; SYMBIOSIS;

ACTINOBACTERIA; ALPHAPROTEOBACTERIA; AMENSALISM; ARTICLE; BACTEROIDETES; CHLOROFLEXI; COMMENSALISM; COMMUNITY DYNAMICS; CONVERGENT EVOLUTION; CRENARCHAEOTA; CYANOBACTERIUM; FIRMICUTES; GAMMAPROTEOBACTERIA; HOST; METAGENOMICS; MICROBIAL COMMUNITY; MICROBIAL DIVERSITY; MICROBIOME; NONHUMAN; ORGANISMAL INTERACTION; PHYLOGENY; PYROSEQUENCING; SEDIMENT; SPECIES COMPOSITION; SPONGE (PORIFERA); SPONGE MICROBIOME; SYMBIONT; ANIMAL; BAYES THEOREM; BIODIVERSITY; CLASSIFICATION; COEVOLUTION; ECOSYSTEM; GENETICS; MICROBIAL CONSORTIUM; MICROBIOLOGY; MICROFLORA; PHYSIOLOGY; SYMBIOSIS;

METAZOA; PORIFERA;

ANIMALS; BAYES THEOREM; BIODIVERSITY; BIOLOGICAL COEVOLUTION; ECOSYSTEM; MICROBIAL CONSORTIA; MICROBIOTA; PHYLOGENY; PORIFERA; RNA, RIBOSOMAL, 16S; SYMBIOSIS;

EID: 84975038062     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms11870     Document Type: Article

References (66)

1. Kau, A. L., Ahern, P. P., Griffin, N. W., Goodman, A. L. & Gordon, J. I. Human nutrition, the gut microbiome and the immune system. Nature 474, 327-336 (2011).
2. Tkacz, A. & Poole, P. Role of root microbiota in plant productivity. J. Exp. Botany 66, 2167-2175 (2015).
3. Cabreiro, F. & Gems, D. Worms need microbes too: microbiota, health and aging in Caenorhabditis elegans. EMBO Mol. Med. 5, 1300-1310 (2013).
4. McFall-Ngai, M. et al. Animals in a bacterial world, a new imperative for the life sciences. Proc. Natl Acad. Sci. USA 110, 3229-3236 (2013).
5. Hacquard, S. et al. Microbiota and host nutrition across plant and animal kingdoms. Cell Host Microbe 17, 603-616 (2015).
6. Hentschel, U., Piel, J., Degnan, S. M. & Taylor, M. W. Genomic insights into the marine sponge microbiome. Nat. Rev. Microbiol. 10, 641-654 (2012).
7. Taylor, M. W., Thacker, R. W. & Hentschel, U. Genetics. Evolutionary insights from sponges. Science (New York, N.Y.) 316, 1854-1855 (2007).
8. Yin, Z. et al. Sponge grade body fossil with cellular resolution dating 60 Myr before the Cambrian. Proc. Natl Acad. Sci. USA 112, E1453-E1460 (2015).
9. Taylor, M. W. et al. 'Sponge-specific' bacteria are widespread (but rare) in diverse marine environments. ISME J. 7, 438-443 (2013).
10. Fan, L. et al. Functional equivalence and evolutionary convergence in complex communities of microbial sponge symbionts. Proc. Natl Acad. Sci. USA 109, E1878-E1887 (2012).
11. de Goeij, J. M. et al. Surviving in a marine desert: the sponge loop retains resources within coral reefs. Science (New York, N.Y.) 342, 108-110 (2013).
12. Taylor, M. W., Radax, R., Steger, D. & Wagner, M. Sponge-associated microorganisms: evolution, ecology, and biotechnological potential. Microbiol. Mol. Biol. Rev. 71, 295-347 (2007).
13. Webster, N. S. et al. Deep sequencing reveals exceptional diversity and modes of transmission for bacterial sponge symbionts. Environ. Microbiol. 12, 2070-2082 (2010).
14. Simister, R. L., Deines, P., Botté, E. S., Webster, N. S. & Taylor, M. W. Sponge-specific clusters revisited: a comprehensive phylogeny of sponge-associated microorganisms. Environ. Microbiol. 14, 517-524 (2012).
15. Human Microbiome Project Consortium. Structure, function and diversity of the healthy human microbiome. Nature 486, 207-214 (2012).
16. Gilbert, J. A., Jansson, J. K. & Knight, R. The Earth Microbiome project: successes and aspirations. BMC Biol. 12, 69 (2014).
17. Thacker, R. W. & Freeman, C. J. Sponge-microbe symbioses: recent advances and new directions. Adv. Mar. Biol. 62, 57 (2012).
18. Vrijenhoek, R. C. in The Vent and Seep Biota 15-49 (Springer, 2010).
19. Dethlefsen, L., McFall-Ngai, M. & Relman, D. A. An ecological and evolutionary perspective on human-microbe mutualism and disease. Nature 449, 811-818 (2007).
20. Schmitt, S. et al. Assessing the complex sponge microbiota: core, variable and species-specific bacterial communities in marine sponges. ISME J. 6, 564-576 (2012).
21. Reveillaud, J. et al. Host-specificity among abundant and rare taxa in the sponge microbiome. ISME J. 8, 1198-1209 (2014).
22. Zinger, L. et al. Global patterns of bacterial beta-diversity in seafloor and seawater ecosystems. PLoS ONE 6, e24570 (2011).
23. Sunagawa, S. et al. Structure and function of the global ocean microbiome. Science (New York, N.Y.) 348, 1261359 (2015).
24. Van Soest, R. W. M. et al. Global diversity of sponges (Porifera). PLoS ONE 7, e35105 (2012).
25. Montoya, J. M., Pimm, S. L. & Sole, R. V. Ecological networks and their fragility. Nature 442, 259-264 (2006).
26. Henderson, P. A. & Magurran, A. E. Direct evidence that density-dependent regulation underpins the temporal stability of abundant species in a diverse animal community. Proc. R. Soc. Lond. B, Biol. Sci. 281, 20141336 (2014).
27. Mutshinda, C. M., O'Hara, R. B. & Woiwod, I. P. What drives community dynamics? Proc. R. Soc. Lond. B, Biol. Sci. 276, 2923-2929 (2009).
28. Erwin, P. M., Pita, L., López-Legentil, S. & Turon, X. Stability of sponge-associated bacteria over large seasonal shifts in temperature and irradiance. Appl. Environ. Microbiol. 78, 7358-7368 (2012).
29. Thébault, E. & Fontaine, C. Stability of ecological communities and the architecture of mutualistic and trophic networks. Science (New York, N.Y.) 329, 853-856 (2010).
30. McCann, K. S. The diversity-stability debate. Nature 405, 228-233 (2000).
31. Rooney, N. & McCann, K. S. Integrating food web diversity, structure and stability. Trends Ecol. Evol. 27, 40-46 (2012).
32. Bastolla, U. et al. The architecture of mutualistic networks minimizes competition and increases biodiversity. Nature 458, 1018-1020 (2009).
33. Lurgi, M., Montoya, D. & Montoya, J. M. The effects of space and diversity of interaction types on the stability of complex ecological networks. Theor. Ecol. 1-11 (2015).
34. Hentschel, U. et al. Molecular evidence for a uniform microbial community in sponges from different oceans. Appl. Environ. Microbiol. 68, 4431-4440 (2002).
35. Moitinho-Silva, L. et al. Specificity and transcriptional activity of microbiota associated with low and high microbial abundance sponges from the Red Sea. Mol. Ecol. 23, 1348-1363 (2014).
36. Costello, E. K., Stagaman, K., Dethlefsen, L., Bohannan, B. J. & Relman, D. A. The application of ecological theory toward an understanding of the human microbiome. Science (New York, N.Y.) 336, 1255-1262 (2012).
37. Easson, C. G. & Thacker, R. W. Phylogenetic signal in the community structure of host-specific microbiomes of tropical marine sponges. Front. Microbiol. 5, 532 (2014).
38. Kembel, S. W. et al. Picante: R tools for integrating phylogenies and ecology. Bioinformatics 26, 1463-1464 (2010).
39. Harmon, L. J., Weir, J. T., Brock, C. D., Glor, R. E. & Challenger, W. GEIGER: investigating evolutionary radiations. Bioinformatics 24, 129-131 (2008).
40. Freeman, C. J., Easson, C. G. & Baker, D. M. Metabolic diversity and niche structure in sponges from the Miskito Cays, Honduras. PeerJ 2, e695 (2014).
41. Faust, K. & Raes, J. Microbial interactions: from networks to models. Nat. Rev. Microbiol. 10, 538-550 (2012).
42. Ramsey, M. M., Rumbaugh, K. P. & Whiteley, M. Metabolite cross-feeding enhances virulence in a model polymicrobial infection. PLoS Pathog 7, e1002012 (2011).
43. Hooper, J. N. & Van Soest, R. W. Systema Porifera. A Guide to the Classification of Sponges (Springer, 2002).
44. Caporaso, J. G. et al. Global patterns of 16 S rRNA diversity at a depth of millions of sequences per sample. Proc. Natl Acad. Sci. USA 108, 4516-4522 (2011).
45. Schloss, P. D. et al. Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl. Environ. Microbiol. 75, 7537-7541 (2009).
46. Quast, C. et al. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res.. gks1219 41, D590-D596 (2012).
47. Quast, C. et al. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res. 41, D590-D596 (2013).
48. Edgar, R. C., Haas, B. J., Clemente, J. C., Quince, C. & Knight, R. UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27, 2194-2200 (2011).
49. Wang, Q., Garrity, G. M., Tiedje, J. M. & Cole, J. R. Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl. Environ. Microbiol. 73, 5261-5267 (2007).
50. Cole, J. R. et al. Ribosomal Database Project: data and tools for high throughput rRNA analysis. Nucleic Acids Res. 42, D633-D642 (2014).
51. DeSantis, T. Z. et al. Greengenes, a chimera-checked 16 S rRNA gene database and workbench compatible with ARB. Appl. Environ. Microbiol. 72, 5069-5072 (2006).
52. Caporaso, J. G. et al. QIIME allows analysis of high-throughput community sequencing data. Nat. Methods 7, 335-336 (2010).
53. Dixon, P. & Palmer, M. VEGAN, a package of R functions for community ecology. J. Veg. Sci. 14, 927-930 (2003).
54. Legendre, P. & Gallagher, E. D. Ecologically meaningful transformations for ordination of species data. Oecologia 129, 271-280 (2001).
55. Simpson, G. L. Analogue Methods in Palaeoecology: Using the analogue Package. J. Stat. Softw. 22, 1-29 (2007).
56. Kolde, R. Pheatmap: pretty heatmaps. R Package Version 61, 1-7 (2012).
57. Csardi, G & Nepusz T The igraph software package for complex network research InterJ. Complex Syst. 1695 1-9 2006.
58. Gentleman, R., Ihaka, R & Leisch, F. R: A Language and Environment for Statistical Computing (Vienna, 2003).
59. O'Hara, R. B. & Sillanpää, M. J. A review of Bayesian variable selection methods: what, how and which. Bayesian Anal. 4, 85-117 (2009).
60. Denwood, M. runjags: An R package providing interface utilities, parallel computing methods and additional distributions for MCMC models in JAGS. J. Stat. Softw. (in review) http://runjags.sourceforge.net (2013).
61. Altschul, S. F. et al. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25, 3389-3402 (1997).
62. Katoh, K., Misawa, K., Kuma, K. & Miyata, T. MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res. 30, 3059-3066 (2002).
63. Castresana, J. Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol. Biol. Evol. 17, 540-552 (2000).
64. 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).
65. Miller, M. A., Pfeiffer, W. & Schwartz, T. in Gateway Computing Environments Workshop (GCE) 1-8 (IEEE, 2010).
66. Huelsenbeck, J. P. & Rannala, B. Frequentist properties of Bayesian posterior probabilities of phylogenetic trees under simple and complex substitution models. Syst. Biol. 53, 904-913 (2004).