Skip to main content

Advertisement

Log in

The coupling of taxonomy and function in microbiomes

  • Published:
Biology & Philosophy Aims and scope Submit manuscript

Abstract

Microbiologists are transitioning from the study and characterization of individual strains or species to the profiling of whole microbiomes and microbial ecology. Equipped with high-throughput methods for studying the taxonomic and functional characteristics of diverse samples, they are just beginning to encounter the conceptual, theoretical, and experimental problems of comparing taxonomy to (micro-ecological) function, and extracting useful measures from such comparisons (i.e. diversity, stability, or “health”). Although still unresolved, these problems are well studied in macro-ecology (the ecology of non-microbes) and are reiterated here as an historical precautionary for microbial ecologists. Beyond expected and unresolved terminological vagueness, we argue that assessments and comparisons of taxonomic and functional profiles in micro-ecology suffer from theoretically unresolvable arbitrariness and ambiguities. We divide these into problems of scale, individuation, and commensurability. We argue that there is no technically/theoretically “correct” scale, individuation, or comparison of taxonomy and function, but there are nonetheless better and worse methodologies for profiling.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Notes

  1. Furthermore, as a reviewer pointed out, metagenomic gene catalogs do not capture gene interaction, thus further complicating the relation between gene presence and phenotypic expression.

References

  • Abubucker S, Segata N, Goll J, Schubert AM, Izard J, Cantarel BL, Rodriguez-Mueller B, Zucker J, Thiagarajan M, Henrissat B, White O (2012) Metabolic reconstruction for metagenomic data and its application to the human microbiome. PLoS Comput Biol 8:e1002358

    Article  Google Scholar 

  • Amend AS, Martiny AC, Allison SD, Berlemont R, Goulden ML, Lu Y, Treseder KK, Weihe C, Martiny JBH (2016) Microbial response to simulated global change is phylogentically conserved and linked with functional potential. ISME J 10:109–118

    Article  Google Scholar 

  • Amundson R, Lauder GV (1994) Function without purpose. Biol Phil 9:443–469

    Article  Google Scholar 

  • Apweiler R, Bairoch A, Wu CH, Barker WC, Boeckmann B, Ferro S, Gasteiger E, Huang H, Lopez R, Magrane M, Martin MJ, Natale DA, O’Donovan C, Redaschi N, Yeh LS (2004) UniProt: the universal protein knowledgebase. Nucleic Acids Res 32:115–119

    Article  Google Scholar 

  • Bäckhed F, Fraser CM, Ringel Y, Sanders ME, Sartour RB, Sherman PM, Versalovic J, Young V, Finlay BB (2012) Defining a healthy human gut microbiome: current concepts, future directions, and clinical applications. Cell Host Microbe 12:611–612

    Article  Google Scholar 

  • Bickle J (2016) Multiple realizability. In: Zalta EN (ed) The Stanford Encyclopedia of Philosophy (Spring). MIT Press, Cambridge

    Google Scholar 

  • Blaser MJ (2014) Missing microbes: How the overuse of antibiotics is fueling our modern plagues. Henry Holt, New York

    Google Scholar 

  • Budinich M, Bourdon J, Larhlimi A, Eveillard D (2017) A multi-objective constraint- based approach for modeling genome-scale microbial ecosystems. PLoS ONE 12:e0171744

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Cadotte MW, Carscadden K, Mirotchnick N (2011) Beyond species: functional diversity and the maintenance of ecological processes and services. J Appl Ecol 48:1079–1087

    Article  Google Scholar 

  • Cardinale BJ, Duffy JE, Gonzalez A, Hooper DU, Perrings C, Venail P, Narwani A, Mace GM, Tilman D, Wardle DA, Kinzig AP (2012) Biodiversity loss and its impact on humanity. Nature 486:59–67

    Article  Google Scholar 

  • Carmona CP, de Bello F, Mason NW, Lepš J (2016) Traits without borders: integrating functional diversity across scales. Trends Ecol Evol 31:382–394

    Article  Google Scholar 

  • Cordero OX, Polz MF (2014) Explaining microbial genomic diversity in light of evolutionary ecology. Nat Rev Microbiol 12:263–273

    Article  Google Scholar 

  • Cummins RC (1975) Functional analysis. J Philos 72:741–764

    Article  Google Scholar 

  • DeLaplante K, Picasso V (2011) The biodiversity-ecosystem function debate in ecology. In: DeLaplante K, Brown B, Peacock KA (eds) Philosophy of ecology. Elsevier, Oxford, pp 219–250

    Google Scholar 

  • Dietert R (2016) The human superorganism: how the microbiome is revolutionizing the pursuit of a healthy life. Dutton, New York

    Google Scholar 

  • Doolittle WF (1999) Phylogenetic classification and the universal tree. Science 284:2124–2128

    Article  Google Scholar 

  • Doolittle WF, Booth A (2017) It’s the song, not the singer: an exploration of holobioisis and evolutionary theory. Biol Philos 32:5

    Article  Google Scholar 

  • Doolittle WF, Zhaxybayeva O (2009) On the origin of prokaryotic species. Genome Res 19(5):744–756

    Article  Google Scholar 

  • Dussault AC, Bouchard F (2017) A persistence enhancing propensity account of ecological function to explain ecosystem evolution. Synthese 194:1115–1145

    Article  Google Scholar 

  • Elton CS (1958) The ecology of invasions by animals and plants. Chapman & Hall, London

    Book  Google Scholar 

  • Enright MC, Robinson DA, Randle G, Feil EJ, Grundmann H, Spratt BG (2002) The evolutionary history of methicillin-resistant Staphylococcus aureus (MRSA). Proc Natl Acad Sci USA 99:7687–7692

    Article  Google Scholar 

  • Gagic V, Bartomeus I, Jonsson T, Taylor A, Winqvist C, Fischer C, Tscharntke T (2015) Functional identity and diversity of animals predict ecosystem functioning better than species-based indices. Proc R Soc Lond B Biol Sci 282:20142620

    Article  Google Scholar 

  • Green JL, Bohannon BJM, Whitaker RJ (2008) Microbial biogeography: from taxonomy to traits. Science 320:1039–1043

    Article  Google Scholar 

  • Hanson CA, Fuhrman JA, Homer-Devine MC, Martiny JB (2012) Beyond biogeographic patterns: processes shaping the microbial landscape. Nat Rev Microbiol 10:497–506

    Article  Google Scholar 

  • Huddleston JR (2014) Horizontal gene transfer in the human gastrointestinal tract: potential spread of antibiotic resistance genes. Infect Drug Resist 7:167–176

    Article  Google Scholar 

  • Human Microbiome Project Consortium (2012) A framework for human microbiome research. Nature 486:215–221

    Article  Google Scholar 

  • Hurlburt S (1971) The nonconcept of species diversity: a critique and alternative parameters. Ecology 52:577–586

    Article  Google Scholar 

  • Ives AR, Carpenter SR (2007) Stability and diversity of ecosystems. Science 317:58–62

    Article  Google Scholar 

  • Jax K (2010) Ecosystem functioning. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Justus J (2011) A case study in concept determination: Ecological diversity. In: DeLaplante K, Brown B, Peacock KA (eds) Philosophy of ecology. Elsevier, Oxford

    Google Scholar 

  • Kanehisa M, Goto S (2000) KEGG: Kyoto encyclopedia of genes and genomes. Nucleic Acids Res 28:27–30

    Article  Google Scholar 

  • Kanehisa M, Sato Y, Kawashima M, Furumichi M, Tanabe M (2016) KEGG as a reference resource for gene and protein annotation. Nucleic Acids Res 44:457–462

    Article  Google Scholar 

  • Krause S, Le Roiux X, Niklaus PA, Van Bodegom PM, Lennon JT, Bertilsson S, Grossart H-P, Philipott L, Bodelier PLE (2014) Trait-based approaches for understanding microbial biodiversity and ecosystem functioning. Front Microbiol 5:251

    Article  Google Scholar 

  • Kuhn TS (1976) The structure of scientific revolutions (Chicago, 1962)

  • Land M, Hauser L, Jun SR, Nookaew I, Leuze MR, Ahn TH, Karpinets T, Lund O, Kora G, Wassenaar T, Poudel S, Ussery DW (2015) Insights from 20 years of bacterial genome sequencing. Funct Integr Genom 15:141–161

    Article  Google Scholar 

  • Langille MGI, Zaneveld J, Caporoso JG, McDonald D, Knights D, Reyes JA, Clemente JC, Burkepile DE, Vega Thurber RI, Knight R, Beiko RG, Huttenhower C (2013) Positive functional profiling of microbial communities using 16S marker gene sequences. Nat Biotech 31:814–821

    Article  Google Scholar 

  • Louca S, Parfrey LW, Doebeli M (2016) Decoupling function and taxonomy in the global ocean genome. Science 353:1272–1277

    Article  Google Scholar 

  • MacArthur RH (1955) Fluctuations of animal populations, and a measure of community stability. Ecology 36:533–536

    Article  Google Scholar 

  • Maclaurin J, Sterelny K (2008) What is biodiversity?. University of Chicago Press, Chicago

    Book  Google Scholar 

  • Manor O, Borenstein E (2017) Systematic characterization and analysis of the taxonomic drivers of functional shifts in the human microbiome. Cell Host Microbe 21:254–267

    Article  Google Scholar 

  • Martiny JBH, Bohannon BJM, Brown JH, Colwell RK, Fuhrman JA, Green JL, Horner-Devine MC, Kane M, Krumins JA, Kuske CR, Morin PJ, Naeem S, Øvreas L, Reysenbach A-L, Smith VH, Staley JT (2006) Microbial biogeography: putting microorganisms on the map. Nat Rev Microbiol 4:102–112

    Article  Google Scholar 

  • Martiny AC, Treseder K, Pusch G (2013) Phylogenetic conservatism of functional traits in microorganisms. ISME J 7:830–838

    Article  Google Scholar 

  • Mason NW, Mouillot D, Lee WG, Wilson JB (2005) Functional richness, functional evenness and functional divergence: the primary components of functional diversity. Oikos 111:112–118

    Article  Google Scholar 

  • May RM (1973) Stability and complexity of model ecosystems. Princeton University Press, Princeton

    Google Scholar 

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

    Article  Google Scholar 

  • Meyer KM, Klein AM, Rodrigues JLM, Nüsskein K, Tringe SG, Mirza BS, Tiedje JM, Bohannonn BJM (2017) Conversion of Amazon rainforest to agriculture alters community traits of methane-cycling organisms. Mol Ecol 26:1547–1556

    Article  Google Scholar 

  • Mikkelson GM (1997) Methods and metaphors in community ecology: the problemof defining stability. Perspect Sci 5:481–498

    Google Scholar 

  • Mlambo MC (2014) Not all traits are ‘functional’: insights from taxonomy and biodiversity-ecosystem functioning research. Biodivers Conserv 23:781–790

    Article  Google Scholar 

  • Mossio M, Saborido C, Moreno A (2009) An organizational account of biological functions. Br J Philos Sci 60:813–841

    Article  Google Scholar 

  • Naeem S (2002) Ecosystem consequences of biodiversity loss: the evolution of a paradigm. Ecology 83:1537

    Article  Google Scholar 

  • Naeem S, Wright JP (2003) Disentangling biodiversity effects on ecosystem functioning: deriving solutions to a seemingly insurmountable problem. Ecol Lett 6:567–579

    Article  Google Scholar 

  • Nunes-Neto N, Moreno A, El-Hani CN (2014) Function in ecology: an organizational approach. Biol Philos 29:123–141

    Article  Google Scholar 

  • O’Malley M (2008) ‘Everything is everywhere: but the environment selects’: ubiquitous distribution and ecological determinism in microbial biogeography. Stud Hist Philos Biol Biomed Sci 39:314–325

    Article  Google Scholar 

  • Odum EP (1953) Fundamentals of ecology. Saunders, Philadelphia

    Google Scholar 

  • Ouzounis CA, Coulson RM, Enright AJ, Kunin V, Pereira-Leal JB (2003) Classification schemes for protein structure and function. Nat Rev Genet 4:508–519

    Article  Google Scholar 

  • Pavlicev M, Cheverud JM (2015) Constraints evolve: context dependency of gene effects allows evolution of pleiotropy. Annu Rev Ecol Evol Syst 46:413–434

    Article  Google Scholar 

  • Petchey OL, Gaston KJ (2006) Functional diversity: back to basics and looking forward. Ecol Lett 9:741–758

    Article  Google Scholar 

  • Petersen C, Round JL (2014) Defining dysbiosis and its influence on host immunity and disease. Cell Microbiol 16:1024–1033

    Article  Google Scholar 

  • Pimm SL (1980) Food web design and the effect of species deletion. Oikos 35:139–149

    Article  Google Scholar 

  • Prakash T, Taylor TD (2012) Functional assignment of metagenomic data: challenges and applications. Brief Bioinform 13:711–727

    Article  Google Scholar 

  • Raymond J, Siebert JL, Staples CR, Blankenship RE (2004) The natural history of nitrogen fixation. Mol Biol Evol 21:541–554

    Article  Google Scholar 

  • Riley MA (1998) Molecular mechanisms of bacteriocin evolution. Annu Rev Genet 32:255–278

    Article  Google Scholar 

  • Rison SC, Hodgman TC, Thornton JM (2000) Comparison of functional annotation schemes for genomes. Funct Integr Genom 1:56–69

    Article  Google Scholar 

  • Ronimus RS, Morgan HW (2001) The biochemical properties and phylogenies of phosphofructokinases from extremophiles. Extremophiles 5:357–373

    Article  Google Scholar 

  • Sarkar S (2007) From ecological diversity to biodiversity. In: Hull D, Ruse M (eds) Cambridge companion to the philosophy of biology. Cambridge University Press, Cambridge

    Google Scholar 

  • Shapiro BJ, Leducq J-B, Mallet J (2016) What is speciation? PLoS Genet 12:e100

    Article  Google Scholar 

  • Sober E (1993) The nature of selection: evolutionary theory in philosophical focus. University of Chicago Press, Chicago

    Google Scholar 

  • Stulberg E, Fravel D, Proctor LM, Murray DM, LoTempio J, Chrisey L, Graber J, Harris MC, Jackson S, Mishkind M, Porterfield M, Records A (2016) Am assessment of US microbiome research. Nat Microbiol 1:1–7

    Article  Google Scholar 

  • The Human Microbiome Consortium (2012) Structure, function and diversity of the healthy human microbiome. Nature 486:207–214

    Article  Google Scholar 

  • Tilman D, Downing JA (1994) Biodiversity and stability in grass-lands. Nature 367:363–365

    Article  Google Scholar 

  • Tilman D, Wedin D, Knops J (1996) Productivity and sustainability influenced by biodiversity in grassland ecosystems. Nature 379:718–720

    Article  Google Scholar 

  • Tringe SG (2005) Comparative metagenomics of microbial communities. Science 308:554–557

    Article  Google Scholar 

  • Turnbaugh PJ, Hamady M, Yatsunenko T, Cantarel BL, Duncan A, Ley RE, Sogin ML, Jones WJ, Roe BA, Affourtit JP, Egholm M (2009) A core gut microbiome in obese and lean twins. Nature 457:480–485

    Article  Google Scholar 

  • Wilson GA, Bertrand N, Patel Y, Hughes JB, Feil EJ, Field D (2005) Orphans as taxonomically restricted and ecologically important genes. Microbiology 151:2499–2501

    Article  Google Scholar 

  • Wright L (1973) Functions. Philos Rev 82:139–168

    Article  Google Scholar 

  • Wright JP, Naeem S, Hector A, Lehman C, Reich PB, Schmid B, Tilman D (2006) Conventional functional classification schemes underestimate the relationship with ecosystem functioning. Ecol Lett 9:111–120

    Article  Google Scholar 

Download references

Acknowledgements

We thank Adam Martiny and an anonymous reviewer for Biology and Philosophy for their very helpful comments. G.M.D. is supported by an NSERC Alexander Graham Bell Canada Graduate Scholarship. W.F.D. is supported by an NSERC Herzberg Medal Grant. M.G.I.L. is supported by an NSERC Discovery Grant.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to S. Andrew Inkpen.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Inkpen, S.A., Douglas, G.M., Brunet, T.D.P. et al. The coupling of taxonomy and function in microbiomes. Biol Philos 32, 1225–1243 (2017). https://doi.org/10.1007/s10539-017-9602-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10539-017-9602-2

Keywords

Navigation