Function and functional redundancy in microbial systems


Microbial communities often exhibit incredible taxonomic diversity, raising questions regarding the mechanisms enabling species coexistence and the role of this diversity in community functioning. On the one hand, many coexisting but taxonomically distinct microorganisms can encode the same energy-yielding metabolic functions, and this functional redundancy contrasts with the expectation that species should occupy distinct metabolic niches. On the other hand, the identity of taxa encoding each function can vary substantially across space or time with little effect on the function, and this taxonomic variability is frequently thought to result from ecological drift between equivalent organisms. Here, we synthesize the powerful paradigm emerging from these two patterns, connecting the roles of function, functional redundancy and taxonomy in microbial systems. We conclude that both patterns are unlikely to be the result of ecological drift, but are inevitable emergent properties of open microbial systems resulting mainly from biotic interactions and environmental and spatial processes.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.


All prices are NET prices.

Fig. 1: Gene-centric structure of microbial communities can decouple from taxonomic composition.
Fig. 2: Phylogenetic conservatism varies between functions and between clades.
Fig. 3: Functional redundancy in methanogenic communities (schematic illustration).


  1. 1.

    Hug, L. A. et al. A new view of the tree of life. Nat. Microbiol. 1, 16048 (2016).

  2. 2.

    Gans, J., Wolinsky, M. & Dunbar, J. Computational improvements reveal great bacterial diversity and high metal toxicity in soil. Science 309, 1387–1390 (2005).

  3. 3.

    Powell, S. et al. eggnog v4.0: nested orthology inference across 3686 organisms. Nucleic Acids Res. 42, D231–D239 (2014).

  4. 4.

    O'Leary, N. A. et al. Reference sequence (RefSeq) database at NCBI: current status, taxonomic expansion, and functional annotation. Nucleic Acids Res. 44, D733–D745 (2016).

  5. 5.

    Falkowski, P. G., Fenchel, T. & Delong, E. F. The microbial engines that drive Earth's biogeochemical cycles. Science 320, 1034–1039 (2008).

  6. 6.

    Raes, J., Letunic, I., Yamada, T., Jensen, L. J. & Bork, P. Toward molecular trait-based ecology through integration of biogeochemical, geographical and metagenomic data. Mol. Syst. Biol. 7, 473 (2011).

  7. 7.

    Reed, D. C., Algar, C. K., Huber, J. A. & Dick, G. J. Gene-centric approach to integrating environmental genomics and biogeochemical models. Proc. Natl Acad. Sci. USA 111, 1879–1884 (2014).

  8. 8.

    Louca, S. et al. Integrating biogeochemistry with multiomic sequence information in a model oxygen minimum zone. Proc. Natl Acad. Sci. USA 113, E5925–E5933 (2016).

  9. 9.

    Louca, S., Parfrey, L. W. & Doebeli, M. Decoupling function and taxonomy in the global ocean microbiome. Science 353, 1272–1277 (2016).

  10. 10.

    Fernández, A. et al. How stable is stable? Function versus community composition. Appl. Environ. Microbiol. 65, 3697–3704 (1999).

  11. 11.

    Turnbaugh, P. J. et al. A core gut microbiome in obese and lean twins. Nature 457, 480–484 (2009).

  12. 12.

    Burke, C., Steinberg, P., Rusch, D., Kjelleberg, S. & Thomas, T. Bacterial community assembly based on functional genes rather than species. Proc. Natl Acad. Sci. USA 108, 14288–14293 (2011).

  13. 13.

    Nelson, M. B., Martiny, A. C. & Martiny, J. B. H. Global biogeography of microbial nitrogen-cycling traits in soil. Proc. Natl Acad. Sci. USA 113, 8033–8040 (2016).

  14. 14.

    Louca, S. et al. High taxonomic variability despite stable functional structure across microbial communities. Nat. Ecol. Evol. 1, 0015 (2016).

  15. 15.

    Wittebolle, L., Vervaeren, H., Verstraete, W. & Boon, N. Quantifying community dynamics of nitrifiers in functionally stable reactors. Appl. Environ. Microbiol. 74, 286–293 (2008).

  16. 16.

    Wells, G. F. et al. Ammonia-oxidizing communities in a highly aerated full-scale activated sludge bioreactor: betaproteobacterial dynamics and low relative abundance of crenarchaea. Environ. Microbiol. 11, 2310–2328 (2009).

  17. 17.

    Vanwonterghem, I., Jensen, P. D., Rabaey, K. & Tyson, G. W. Genome-centric resolution of microbial diversity, metabolism and interactions in anaerobic digestion. Environ. Microbiol. 18, 3144–3158 (2016).

  18. 18.

    Anantharaman, K. et al. Thousands of microbial genomes shed light on interconnected biogeochemical processes in an aquifer system. Nat. Commun. 7, 13219 (2016).

  19. 19.

    Tringe, S. G. et al. Comparative metagenomics of microbial communities. Science 308, 554–557 (2005).

  20. 20.

    Kaewpipat, K. & Grady, C. Microbial population dynamics in laboratory-scale activated sludge reactors. Water Sci. Technol. 46, 19–27 (2002).

  21. 21.

    Wang, X. et al. Bacterial community dynamics in a functionally stable pilot-scale wastewater treatment plant. Bioresour. Technol. 102, 2352–2357 (2011).

  22. 22.

    Fernandez-Gonzalez, N., Huber, J. A. & Vallino, J. J. Microbial communities are well adapted to disturbances in energy input. mSystems 1, e00117-16 (2016).

  23. 23.

    Sheng, Y. et al. Geochemical and temporal influences on the enrichment of acidophilic iron-oxidizing bacterial communities. Appl. Environ. Microbiol. 82, 3611–3621 (2016).

  24. 24.

    Aguilar, D., Aviles, F. X., Querol, E. & Sternberg, M. J. E. Analysis of phenetic trees based on metabolic capabilites across the three domains of life. J. Mol. Biol. 340, 491–512 (2004).

  25. 25.

    Martiny, J. B. H., Jones, S. E., Lennon, J. T. & Martiny, A. C. Microbiomes in light of traits: a phylogenetic perspective. Science 350, aac9323 (2015).

  26. 26.

    Morris, J. J., Lenski, R. E. & Zinser, E. R. The black queen hypothesis: evolution of dependencies through adaptive gene loss. MBio 3, e00036–12 (2012).

  27. 27.

    David, L. A. & Alm, E. J. Rapid evolutionary innovation during an Archaean genetic expansion. Nature 469, 93–96 (2011).

  28. 28.

    Hehemann, J. H. et al. Adaptive radiation by waves of gene transfer leads to fine-scale resource partitioning in marine microbes. Nat. Commun. 7, 12860 (2016).

  29. 29.

    Welch, R. A. et al. Extensive mosaic structure revealed by the complete genome sequence of uropathogenic Escherichia coli. Proc. Natl Acad. Sci. USA 99, 17020–17024 (2002).

  30. 30.

    Martiny, A. C., Treseder, K. & Pusch, G. Phylogenetic conservatism of functional traits in microorganisms. ISME J. 7, 830–838 (2013).

  31. 31.

    Whitman, W. B. (ed.) Bergey's Manual of Systematics of Archaea and Bacteria.(John Wiley & Sons, Hoboken, 2015).

  32. 32.

    Canfield, D. E. & Thamdrup, B. Towards a consistent classification scheme for geochemical environments, or, why we wish the term ‘suboxic’ would go away. Geobiology 7, 385–392 (2009).

  33. 33.

    Reed, D. C. et al. Predicting the response of the deep-ocean microbiome to geochemical perturbations by hydrothermal vents. ISME J. 9, 1857–1869 (2015).

  34. 34.

    Graham, E. B. et al. Microbes as engines of ecosystem function: when does community structure enhance predictions of ecosystem processes? Front. Microbiol. 7, 214 (2016).

  35. 35.

    Girvan, M. S., Campbell, C. D., Killham, K., Prosser, J. I. & Glover, L. A. Bacterial diversity promotes community stability and functional resilience after perturbation. Environ. Microbiol. 7, 301–313 (2005).

  36. 36.

    Langenheder, S., Lindström, E. S. & Tranvik, L. J. Weak coupling between community composition and functioning of aquatic bacteria. Limnol. Oceanogr. 50, 957–967 (2005).

  37. 37.

    Langenheder, S., Lindström, E. S. & Tranvik, L. J. Structure and function of bacterial communities emerging from different sources under identical conditions. Appl. Environ. Microbiol. 72, 212–220 (2006).

  38. 38.

    Peter, H. et al. Function-specific response to depletion of microbial diversity. ISME J. 5, 351–361 (2011).

  39. 39.

    Jurburg, S. D. & Salles, J. F. in Biodiversity in Ecosystems - Linking Structure and Function (eds Lo, Y.-H., Blanco, J. A. & Roy, S.) Ch. 2, 29–49 (INTECH, 2015).

  40. 40.

    Louca, S. & Doebeli, M. Taxonomic variability and functional stability in microbial communities infected by phages. Environ. Microbiol. 19, 3863–3878 (2017).

  41. 41.

    Hawley, A. K., Brewer, H. M., Norbeck, A. D., Paša-Tolić, L. & Hallam, S. J. Metaproteomics reveals differential modes of metabolic coupling among ubiquitous oxygen minimum zone microbes. Proc. Natl Acad. Sci. USA 111, 11395–11400 (2014).

  42. 42.

    Lavorel, S. & Garnier, E. Predicting changes in community composition and ecosystem functioning from plant traits: revisiting the holy grail. Funct. Ecol. 16, 545–556 (2002).

  43. 43.

    Tully, B., Wheat, C. G., Glazer, B. T. & Huber, J. A dynamic microbial community with high functional redundancy inhabits the cold, oxic subseafloor aquifer. ISME J. 12, 1–16 (2017).

  44. 44.

    Kashtan, N. et al. Single-cell genomics reveals hundreds of coexisting subpopulations in wild Prochlorococcus. Science 344, 416–420 (2014).

  45. 45.

    Fuhrman, J. A., Cram, J. A. & Needham, D. M. Marine microbial community dynamics and their ecological interpretation. Nat. Rev. Microbiol 13, 133–146 (2015).

  46. 46.

    Allison, S. D. & Martiny, J. B. H. Resistance, resilience, and redundancy in microbial communities. Proc. Natl Acad. Sci. USA 105, 11512–11519 (2008).

  47. 47.

    Chesson, P. Mechanisms of maintenance of species diversity. Annu. Rev. Ecol. Syst. 31, 343–366 (2000).

  48. 48.

    Tilman, D. Resource Competition and Community Structure (Princeton Univ. Press, Princeton, 1982).

  49. 49.

    Freter, R., Brickner, H., Botney, M., Cleven, D. & Aranki, A. Mechanisms that control bacterial populations in continuous-flow culture models of mouse large intestinal flora. Infect. Immun. 39, 676–685 (1983).

  50. 50.

    Yawata, Y. et al. Competition–dispersal tradeoff ecologically differentiates recently speciated marine bacterioplankton populations. Proc. Natl Acad. Sci. USA 111, 5622–5627 (2014).

  51. 51.

    Pereira, F. C. & Berry, D. Microbial nutrient niches in the gut. Environ. Microbiol. 19, 1366–1378 (2017).

  52. 52.

    Sommer, U. The paradox of the plankton: Fluctuations of phosphorus availability maintain diversity of phytoplankton in flow-through cultures. Limnol. Oceanogr. 29, 633–636 (1984).

  53. 53.

    Moore, C. et al. Processes and patterns of oceanic nutrient limitation. Nat. Geosci. 6, 701–710 (2013).

  54. 54.

    Wildschutte, H., Wolfe, D. M., Tamewitz, A. & Lawrence, J. G. Protozoan predation, diversifying selection, and the evolution of antigenic diversity in salmonella. Proc. Natl Acad. Sci. USA 101, 10644–10649 (2004).

  55. 55.

    Rodriguez-Valera, F. et al. Explaining microbial population genomics through phage predation. Nat. Rev. Microbiol. 7, 828–836 (2009).

  56. 56.

    Bohannan, B. J. M., Kerr, B., Jessup, C. M., Hughes, J. B. & Sandvik, G. Trade-offs and coexistence in microbial microcosms. Antonie Leeuwenhoek 81, 107–115 (2002).

  57. 57.

    Chesson, P. & Kuang, J. J. The interaction between predation and competition. Nature 456, 235–238 (2008).

  58. 58.

    Cordero, O. X. & Polz, M. F. Explaining microbial genomic diversity in light of evolutionary ecology. Nat. Rev. Microbiol. 12, 263–273 (2014).

  59. 59.

    Czárán, T. L., Hoekstra, R. F. & Pagie, L. Chemical warfare between microbes promotes biodiversity. Proc. Natl Acad. Sci. USA 99, 786–790 (2002).

  60. 60.

    Hibbing, M. E., Fuqua, C., Parsek, M. R. & Peterson, S. B. Bacterial competition: surviving and thriving in the microbial jungle. Nat. Rev. Microbiol. 8, 15–25 (2010).

  61. 61.

    Hutchinson, G. Concluding remarks. Cold Spring Harb. Symp. Quant. Biol. 22, 415–427 (1957).

  62. 62.

    Plichta, D. R. et al. Transcriptional interactions suggest niche segregation among microorganisms in the human gut. Nat. Microbiol. 1, 16152 (2016).

  63. 63.

    Loreau, M. Does functional redundancy exist? Oikos 104, 606–611 (2004).

  64. 64.

    Curtis, T. P. & Sloan, W. T. Prokaryotic diversity and its limits: microbial community structure in nature and implications for microbial ecology. Curr. Opin. Microbiol. 7, 221–226 (2004).

  65. 65.

    Konopka, A., Lindemann, S. & Fredrickson, J. Dynamics in microbial communities: unraveling mechanisms to identify principles. ISME J. 9, 1488–1495 (2015).

  66. 66.

    Hubbell, S. P. The Unified Neutral Theory of Biodiversity and Biogeography Vol. 32 (Princeton Univ. Press, Princeton, 2001).

  67. 67.

    Sloan, W. T. et al. Quantifying the roles of immigration and chance in shaping prokaryote community structure. Environ. Microbiol. 8, 732–740 (2006).

  68. 68.

    Sloan, W. T., Woodcock, S., Lunn, M., Head, I. M. & Curtis, T. P. Modeling taxa-abundance distributions in microbial communities using environmental sequence data. Microb. Ecol. 53, 443–455 (2007).

  69. 69.

    Burns, A. R. et al. Contribution of neutral processes to the assembly of gut microbial communities in the zebrafish over host development. ISME J. 10, 655–664 (2015).

  70. 70.

    Dumbrell, A. J., Nelson, M., Helgason, T., Dytham, C. & Fitter, A. H. Relative roles of niche and neutral processes in structuring a soil microbial community. ISME J. 4, 337–345 (2009).

  71. 71.

    Curtis, T., Polchan, M., Baptista, J., Davenport, R. & Sloan, W. Microbial community assembly, theory and rare functions. Front. Microbiol. 4, 68 (2013).

  72. 72.

    Woodcock, S. et al. Neutral assembly of bacterial communities. FEMS Microbiol. Ecol. 62, 171–180 (2007).

  73. 73.

    Woodcock, S. & Sloan, W. T. Biofilm community succession: a neutral perspective. Microbiology 163, 664–668 (2017).

  74. 74.

    Ayarza, J. M. & Erijman, L. Balance of neutral and deterministic components in the dynamics of activated sludge floc assembly. Microb. Ecol. 61, 486–495 (2010).

  75. 75.

    Ofiţeru, I. D. et al. Combined niche and neutral effects in a microbial wastewater treatment community. Proc. Natl Acad. Sci. USA 107, 15345–15350 (2010).

  76. 76.

    Stegen, J. C., Lin, X., Konopka, A. E. & Fredrickson, J. K. Stochastic and deterministic assembly processes in subsurface microbial communities. ISME J. 6, 1653–1664 (2012).

  77. 77.

    Frossard, A., Gerull, L., Mutz, M. & Gessner, M. O. Disconnect of microbial structure and function: enzyme activities and bacterial communities in nascent stream corridors. ISME J. 6, 680–691 (2012).

  78. 78.

    Lande, R., Engen, S. & Sæther, B. Stochastic Population Dynamics in Ecology and Conservation (Oxford Univ. Press, Oxford, 2003).

  79. 79.

    Vellend, M. Conceptual synthesis in community ecology. Q. Rev. Biol. 85, 183–206 (2010).

  80. 80.

    Krakat, N., Westphal, A., Schmidt, S. & Scherer, P. Anaerobic digestion of renewable biomass: thermophilic temperature governs methanogen population dynamics. Appl. Environ. Microbiol. 76, 1842–1850 (2010).

  81. 81.

    Ohtsubo, S. et al. Comparison of acetate utilization among strains of an aceticlastic methanogen. Methanothrix soehngenii. Appl. Environ. Microbiol. 58, 703–705 (1992).

  82. 82.

    Li, L. & Ma, Z. S. Testing the neutral theory of biodiversity with human microbiome datasets. Sci. Rep. 6, 31448 (2016).

  83. 83.

    Dini-Andreote, F., Stegen, J. C., van Elsas, J. D. & Salles, J. F. Disentangling mechanisms that mediate the balance between stochastic and deterministic processes in microbial succession. Proc. Natl Acad. Sci. USA 112, E1326–E1332 (2015).

  84. 84.

    Albright, M. B. N. & Martiny, J. B. H. Dispersal alters bacterial diversity and composition in a natural community. ISME J. 12, 296–299 (2018).

  85. 85.

    Martiny, J. B. H. et al. Microbial biogeography: putting microorganisms on the map. Nat. Rev. Microbiol. 4, 102–112 (2006).

  86. 86.

    Martiny, J. B. H., Eisen, J. A., Penn, K., Allison, S. D. & Horner-Devine, M. C. Drivers of bacterial β-diversity depend on spatial scale. Proc. Natl Acad. Sci. USA 108, 7850–7854 (2011).

  87. 87.

    Horner-Devine, M. C., Lage, M., Hughes, J. B. & Bohannan, B. J. A taxa–area relationship for bacteria. Nature 432, 750–753 (2004).

  88. 88.

    Vanwonterghem, I. et al. Deterministic processes guide long-term synchronised population dynamics in replicate anaerobic digesters. ISME J. 8, 2015–2028 (2014).

  89. 89.

    Shapiro, O. H. & Kushmaro, A. Bacteriophage ecology in environmental biotechnology processes. Curr. Opin. Biotechnol. 22, 449–455 (2011).

  90. 90.

    Herron, M. D. & Doebeli, M. Parallel evolutionary dynamics of adaptive diversification in Escherichia coli. PLoS Biol. 11, e1001490 (2013).

  91. 91.

    Callahan, B. J., Fukami, T. & Fisher, D. S. Rapid evolution of adaptive niche construction in experimental microbial populations. Evolution 68, 3307–3316 (2014).

  92. 92.

    Graham, D. W. et al. Experimental demonstration of chaotic instability in biological nitrification. ISME J. 1, 385–393 (2007).

  93. 93.

    Fukami, T., Martijn Bezemer, T., Mortimer, S. R. & Putten, W. H. Species divergence and trait convergence in experimental plant community assembly. Ecol. Lett. 8, 1283–1290 (2005).

  94. 94.

    McGill, B. J., Enquist, B. J., Weiher, E. & Westoby, M. Rebuilding community ecology from functional traits. Trends Ecol. Evol. 21, 178–185 (2006).

Download references


We thank M. Pennell, F. Doolittle, A. C. Martiny and I. Rubin for discussions and for participation at a workshop from which this Perspective emerged. We thank the Canadian Institute for Ecology and Evolution (CIEE) for financial support of all authors, by means of a Thematic Working Group grant on the ‘evolution of microbial metabolic and genomic diversity at multiple scales’. We thank the Biodiversity Research Centre and the Adapting Biosystems programme, University of British Columbia, for financial support, and K. Beall for logistical support. S.L. was supported by an NSERC grant and a postdoctoral fellowship from the Biodiversity Research Centre, UBC. J.A.H. was supported by the NSF Center for Dark Energy Biosphere Investigations (OCE-0939564).

Author information




S.L., L.W.P. and M.D. organized the workshop from which this Perspective emerged. S.L. performed the data analyses. All authors contributed to the writing of the manuscript.

Corresponding author

Correspondence to Stilianos Louca.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Supplementary Information

Supplementary Methods, Supplementary Table 1, Supplementary References

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Louca, S., Polz, M.F., Mazel, F. et al. Function and functional redundancy in microbial systems. Nat Ecol Evol 2, 936–943 (2018).

Download citation

Further reading