Skip to main content

Advertisement

Log in

Sketching the Human Microbiome Biogeography with DAR (Diversity-Area Relationship) Profiles

  • Human Microbiome
  • Published:
Microbial Ecology Aims and scope Submit manuscript

Abstract

SAR (species area relationship) is a classic ecological theory that has been extensively investigated and applied in the studies of global biogeography and biodiversity conservation in macro-ecology. It has also found important applications in microbial ecology in recent years thanks to the breakthroughs in metagenomic sequencing technology. Nevertheless, SAR has a serious limitation for practical applications—ignoring the species abundance and treating all species as equally abundant. This study aims to explore the biogeography discoveries of human microbiome over 18 sites of 5 major microbiome habitats, establish the baseline DAR (diversity-area scaling relationship) parameters, and perform comparisons with the classic SAR. The extension from SAR to DAR by adopting the Hill numbers as diversity measures not only overcomes the previously mentioned flaw of SAR but also allows for obtaining a series of important findings on the human microbiome biodiversity and biogeography. Specifically, two types of DAR models were built, the traditional power law (PL) and power law with exponential cutoff (PLEC), using comprehensive datasets from the HMP (human microbiome project). Furthermore, the biogeography “maps” for 18 human microbiome sites using their DAR profiles for assessing and predicting the diversity scaling across individuals, PDO profiles (pair-wise diversity overlap) for measuring diversity overlap (similarity), and MAD profile (for predicting the maximal accrual diversity in a population) were sketched out. The baseline biogeography maps for the healthy human microbiome diversity can offer guidelines for conserving human microbiome diversity and investigating the health implications of the human microbiome diversity and heterogeneity.

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.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  1. Baas-Becking LGM (1934) Geobiologie of inleiding tot de milieukunde. (eds) W.P. Van Stockum & Zoon N.V, Den Haag [Netherlands]

  2. Barberán A, Casamayor EO, Fierer N (2014) The microbial contribution to macroecology. Front Microbiol 5:203. https://doi.org/10.3389/fmicb.2014.00203

    Article  PubMed  PubMed Central  Google Scholar 

  3. Borody TJ, Paramsothy S, Agrawal G (2013) Fecal microbiota transplantation: indications, methods, evidence, and future directions. Curr Gastroenterol Rep 15:337–343

    Article  PubMed  PubMed Central  Google Scholar 

  4. Chao A, Chiu CH, Hsieh TC (2012) Proposing a resolution to debates on diversity partitioning. Ecology 93(9):2037–2051

    Article  PubMed  Google Scholar 

  5. Chao A, Chiu CH, Jost L (2014b) Unifying species diversity, phylogenetic diversity, functional diversity and related similarity and differentiation measures through Hill numbers. Annu Rev Ecol Evol Syst 45:297–324

    Article  Google Scholar 

  6. Chao A, Gotelli NJ, Hsieh TC, Sander EL, Ma KH, Colwell RK, Ellison AM (2014a) Rarefaction and extrapolation with Hill numbers: a framework for sampling and estimation in species diversity studies. Ecol Monogr 84:45–67

    Article  Google Scholar 

  7. Costello EK, Stagaman K, Dethlefsen L, Bohannan BJM, Relman DA (2012) The application of ecological theory toward an understanding of the human microbiome. Science 336:1255–1262

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Dickson RP, Erb-Downward JR, Freeman CM, McCloskey L, Beck JM, Huffnagle GB, Curtis JL (2015) Spatial variation in the healthy human lung microbiome and the adapted island model of lung biogeography. Ann Am Thorac Soc 12(6):821–830

    Article  PubMed  PubMed Central  Google Scholar 

  9. Drakare S, Lennon JJ, Hillebrand H (2006) The imprint of the geographical, evolutionary and ecological context on species–area relationships. Ecol Lett 9:215–227

    Article  PubMed  Google Scholar 

  10. Ellison AM (2010) Partitioning diversity. Ecology 91:1962–1963

    Article  PubMed  Google Scholar 

  11. Fierer N. (2008). Microbial biogeography: patterns in microbial diversity across space and time. In: Accessing uncultivated microorganisms: from the environment to organisms and genomes and back. Zengler K. (editor). ASM Press, Washington DC pgs. 95–115

  12. Gotelli NJ. Chao A (2013) Measuring and estimating species richness, species diversity, and biotic similarity from sampling data. In: Levin SA (ed) Encyclopedia of biodiversity, vol 5, 2nd ed. Academic Press, p 195–211

  13. Green J, Bohannan BJM (2006) Spatial scaling of microbial biodiversity. Trends Ecol Evol 21(9):501–507

    Article  PubMed  Google Scholar 

  14. Haegeman B, Hamelin J, Moriarty J, Neal P, Dushoff J, Weitz JS (2013) Robust estimation of microbial diversity in theory and in practice. ISME J 7:1092–1101

    Article  PubMed  PubMed Central  Google Scholar 

  15. Hanson CA, Fuhrman JA, Claire Horner-Devine M, Martiny JBH (2012) Beyond biogeographic patterns: process shaping the microbial landscape. Nat Rev Microbiol 10:497–506

    Article  CAS  PubMed  Google Scholar 

  16. Harte J, Smith AB, Storch D (2009) Biodiversity scales from plots to biomes with a universal species-area curve. Ecol Lett 12:789–797

    Article  PubMed  Google Scholar 

  17. He FL, Hubbell SP (2011) Species–area relationships always overestimate extinction rates from habitat loss. Nature 473:368–371

    Article  CAS  PubMed  Google Scholar 

  18. Helmus MR, Mahler DL, Losos JB (2014) Island biogeography of the Anthropocene. Nature 513:543–547

    Article  CAS  PubMed  Google Scholar 

  19. Hill MO (1973) Diversity and evenness: a unifying notation and its consequences. Ecology 54:427–342

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  21. Jones SE, Cadkin TA, Newton RJ, McMahon KD (2012) Spatial and temporal scales of aquatic bacteria beta diversity. Front Microbiol 318:64–73

    Google Scholar 

  22. Jost L (2007) Partitioning diversity into independent alpha and beta components. Ecology 88:2427–2439

    Article  PubMed  Google Scholar 

  23. Lomolino MV (2000) Ecology’s most general, yet protean pattern: the species–area relationship. J Biogeogr 27:17–26

    Article  Google Scholar 

  24. Lozupone CA, Stombaugh JI, Gordon JI, Jansson JK, Knight R (2012) Diversity, stability and resilience of the human gut microbiota. Nature 489:220–230

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Ma ZS (2018) DAR (diversity–area relationship): extending classic SAR (species–area relationship) for biodiversity and biogeography. Ecol Evol. https://doi.org/10.1002/ece3.4425

  26. Ma ZS (2015) Power law analysis of the human microbiome. Mol Ecol 24:5428–5445

    Article  PubMed  Google Scholar 

  27. Martiny JBH, Bohannan JM, Brown JH, Robert K, Colwell RK et al (2006) Microbial biogeography: putting microorganisms on the map. Nat Rev Microbiol 4:102–112. https://doi.org/10.1038/nrmicro1341

    Article  CAS  PubMed  Google Scholar 

  28. Noguez AM, Arita HT, Escalante AE, Forney LJ, García-Oliva F, Souza V (2005) Microbial macroecology: highly structured prokaryotic soil assemblages in a tropical deciduous forest. Glob Ecol Biogeogr 14:241–248

    Article  Google Scholar 

  29. O’Doherty KC, Neufeld JD, Brinkman FSL, Gardner H, Guttman DS, Beiko RG (2014) Opinion: conservation and stewardship of the human microbiome. PNAS 111(40):14312–14313

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Oh J, Byrd AL, Deming C, Conlan S, Kong HH, Segre JA (2014) Biogeography and individuality shape function in the human skin metagenome. Nature 514:59–64

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Peay KG, Bruns TD, Kennedy PG, Bergemann SE, Garbelotto M (2007) A strong species–area relationship for eukaryotic soil microbes: island size matters for ectomycorrhizal fungi. Ecol Lett 10:470–480

    Article  PubMed  Google Scholar 

  32. Plotkin JB, Potts MD, Yu DW, Bunyavejchewin S, Condit R, Foster R, Hubbell S, LaFrankie J, Manokaran N, Lee HS, Sukumar R, Nowak MA, Ashton PS (2000) Predicting species diversity in tropical forests. Proc Natl Acad Sci U S A 97:10850–10854

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Ristova PP, Wenzhöfer F, Ramette A, Felden J, Boetius A (2014) Spatial scales of bacterial community diversity at cold seeps (Eastern Mediterranean Sea). ISME J 9:1306–1318

    Article  Google Scholar 

  34. Rosenzweig ML (1995) Species diversity in space and time. Cambridge University Press, Cambridge

    Book  Google Scholar 

  35. Ruff SE, Biddle JF, Teske AP, Knittel K, Boetius A, Ramette A (2015) Global dispersion and local diversification of the methane seep microbiome. Proc Natl Acad Sci 112:4015–4020

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Scheiner SM (2003) Six types of species–area curves. Glob Ecol Biogeogr 12:441–447

    Article  Google Scholar 

  37. Scheiner SM, Chiarucci A, Fox GA, Helmus MR, McGlinn DJ, Willig MR (2011) The underpinnings of the relationship of species richness with space and time. Ecol Monogr 81(2):195–213

    Article  Google Scholar 

  38. Sizling AL, Kunin WE, Sizlingova E, Reif J, Storch D (2011) Between geometry and biology: the problem if universality of the species-area relationship. Am Nat 178(5):602–611

    Article  PubMed  Google Scholar 

  39. Storch D, Keil P, Jetz W (2012) Universal species–area and endemics–area relationships at continental scales. Nature 488:78–83

    Article  CAS  PubMed  Google Scholar 

  40. Tjørve E (2009) Shapes and functions of species–area curves (II): a review of new models and parameterizations. J Biogeogr 36:1435–1445

    Article  Google Scholar 

  41. Tjørve E, Tjørve KMC (2008) The species–area relationship, self-similarity, and the true meaning of the z-value. Ecology 89:3528–3533

    Article  PubMed  Google Scholar 

  42. Triantis KA, Guilhaumon F, Whittaker RJ (2012) The island species–area relationship: biology and statistics. J Biogeogr 39:215–231

    Article  Google Scholar 

  43. Turnbaugh PJ, Ley RE, Hamady M, Fraser-Liggett CM, Knight R, Gordon JI (2007) The human microbiome project. Nature 449:804–810

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Ulrich W, Buszko J (2003) Self-similarity and the species–area relation of Polish butterflies. Basic Appl Ecol 4:263–270

    Article  Google Scholar 

  45. van der Gast CJ (2013) Microbial biogeography and what Baas Becking should have said. Microbiol Today 40:108–111

    Google Scholar 

  46. van der Gast CJ (2015) Microbial biogeography: the end of the ubiquitous dispersal hypothesis? Environ Microbiol 17:544–546. https://doi.org/10.1111/1462-2920.12635

    Article  PubMed  Google Scholar 

  47. White EP et al (2006) A comparison of the species taxonomic groups. Oikos 112:185–195

    Article  Google Scholar 

  48. Whiteson KL, Bailey B, Bergkessel M, Conrad D, Delhaes L, Felts B, Harris JK, Hunter R, Lim YW, Maughan H, Quinn R, Salamon P, Sullivan J, Wagner BD, Rainey PB (2014) The upper respiratory tract as a microbial source for pulmonary infections in cystic fibrosis: parallels from island biogeography. Am J Respir Crit Care Med 189:1309–1315

    Article  PubMed  PubMed Central  Google Scholar 

  49. Whittaker RJ, Triantis KA (2012) The species–area relationship: an exploration of that ‘most general, yet protean pattern’. J Biogeogr 39:623–626

    Article  Google Scholar 

  50. Williams MR, Lamont BB, Henstridge JD (2009) Species–area functions revisited. J. Biogeogr. 36:1994–2004

    Article  Google Scholar 

  51. Ye CX, Hill C, Ruan J, Ruan, Ma ZS (2016) DBG2OLC: efficient assembly of large genomes using Iong erroneous reads of the third generation sequencing technologies. http://www.nature.com/articles/srep31900

  52. Zhou Y, Gao H, Mihindukulasuriya KA, La Rosa PS, Wylie KM, Vishnivetskaya T et al (2013) Biogeography of the ecosystems of the healthy human body. Genome Biol 14:R1

    Article  PubMed  PubMed Central  Google Scholar 

  53. Zinger L, Boetius A, Ramette A (2014) Bacterial taxa–area and distance–decay relationships in marine environments. Mol Ecol 23:954–964

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

I am indebted to DD Ye, LW Li, and J. Li, from the Chinese Academy of Sciences, for their computational help.

Funding

This study received funding from the following sources: National Science Foundation of China (Grant No. 71473243) and Yun-Ridge Industry Technology Leader Grant, a China-US International Cooperation Project on Genomics/Metagenomics Big Data.

Author information

Authors and Affiliations

Authors

Contributions

ZS Ma designed and conducted the study and wrote the paper. The author read and approved the final manuscript for submission.

Corresponding author

Correspondence to Zhanshan (Sam) Ma.

Ethics declarations

Conflict of Interest

The author declares that he has no conflict of interest.

Permit

No permission is needed since the datasets involved in this study were already published and publically available at http://hmpdacc.org.

Electronic Supplementary Material

Supplementary Information includes supplements to Materials and Methods as well as Suppl. Tables S1-S5.

ESM 1

(PDF 832 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ma, Z.(. Sketching the Human Microbiome Biogeography with DAR (Diversity-Area Relationship) Profiles. Microb Ecol 77, 821–838 (2019). https://doi.org/10.1007/s00248-018-1245-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00248-018-1245-6

Keywords

Navigation