Abstract
Ecologists have long studied primary succession, the changes that occur in biological communities after initial colonization of an environment. Most of this work has focused on succession in plant communities, laying the conceptual foundation for much of what we currently know about community assembly patterns over time. Because of their prevalence and importance in ecosystems, an increasing number of studies have focused on microbial community dynamics during succession. Here, we conducted a meta-analysis of bacterial primary succession patterns across a range of distinct habitats, including the infant gut, plant surfaces, soil chronosequences, and aquatic environments, to determine whether consistent changes in bacterial diversity, community composition, and functional traits are evident over the course of succession. Although these distinct habitats harbor unique bacterial communities, we were able to identify patterns in community assembly that were shared across habitat types. We found an increase in taxonomic and functional diversity with time while the taxonomic composition and functional profiles of communities became less variable (lower beta diversity) in late successional stages. In addition, we found consistent decreases in the rRNA operon copy number and in the high-efficient phosphate assimilation process (Pst system) suggesting that reductions in resource availability during succession select for taxa adapted to low-resource conditions. Together, these results highlight that, like many plant communities, microbial communities also exhibit predictable patterns during primary succession.
Similar content being viewed by others
Log in or create a free account to read this content
Gain free access to this article, as well as selected content from this journal and more on nature.com
or
References
Cowles HC. The ecological relations of the vegetation on the sand dunes of Lake Michigan. BotGaz. 1899;27:97–117. 167–902, 281–308, 361–91.
Margalef R. Diversity, stability and maturity in natural ecosystems. In: Van Dobben WH, Lowe-McConnell RH, editors. Unifying concepts in ecology SE–12. The Netherlands: Springer; 1975. pp. 151–60.
Odum EP. The strategy of ecosystem development. Science. 1969;164:262–70.
Connell JH, Slatyer RO. Mechanisms of succession in natural communities and their role in community stability and organization. Am Nat. 1977;111:1119–44.
Maignien L, Deforce EA, Chafee ME, Eren AM, Simmons SL. Ecological succession and stochastic variation in the assembly of Arabidopsis thaliana phyllosphere communities. MBio. 2014;5. e-pub ahead of print https://doi.org/10.1128/mBio.00682-13.
Redford AJ, Fierer N. Bacterial succession on the leaf surface: a novel system for studying successional dynamics. Microb Ecol. 2009;58:189–98.
Shade A, S. McManus P, Handelsman J. Unexpected diversity during community succession in the apple. MBio. 2013;4:e00602–12.
Mushegian AA, Peterson CN, Baker CCM, Pringle A. Bacterial diversity across individual lichens. Appl Environ Microbiol. 2011;77:4249–52.
Fernández-Martínez MA, Pointing SB, Pérez-Ortega S, Arróniz-Crespo M, Green TGA, Rozzi R, et al. Functional ecology of soil microbial communities along a glacier forefield in Tierra del Fuego (Chile). Int Microbiol. 2017;19:161–73.
Brown SP, Jumpponen A. Contrasting primary successional trajectories of fungi and bacteria in retreating glacier soils. Mol Ecol. 2013;23:481–97.
Wei STS, Fernandez-Martinez MA, Chan Y, Van Nostrand JD, de los Rios-Murillo A, Chiu JMY, et al. Diverse metabolic and stress-tolerance pathways in chasmoendolithic and soil communities of Miers Valley, McMurdo Dry Valleys, Antarctica. Polar Biol. 2015;38:433–43.
Koenig JE, Spor A, Scalfone N, Fricker AD, Stombaugh J, Knight R, et al. Succession of microbial consortia in the developing infant gut microbiome. Proc Natl Acad Sci USA. 2011;108:4578–85.
Foxman B, Wu J, Farrer EC, Goldberg DE, Younger JG, Xi C. Early development of bacterial community diversity in emergently placed urinary catheters. BMC Res Notes. 2012;5:332.
Jessup CM, Kassen R, Forde SE, Kerr B, Buckling A, Rainey PB, et al. Big questions, small worlds: microbial model systems in ecology. Trends Ecol Evol. 2004;19:189–97.
Fernández-Martínez MA, Pérez-Ortega S, Pointing SB, Green TGA, Pintado A, Rozzi R et al. Microbial succession dynamics along glacier forefield chronosequences in Tierra del Fuego (Chile). Polar Biol. 2017. e-pub ahead of print https://doi.org/10.1007/s00300-017-2110-7.
Nemergut DR, Schmidt SK, Fukami T, O’Neill SP, Bilinski TM, Stanish LF, et al. Patterns and processes of microbial community assembly. Microbiol Mol Biol Rev. 2013;77:342–56.
Kreyling J, Jentsch A, Beierkuhnlein C. Stochastic trajectories of succession initiated by extreme climatic events. Ecol Lett. 2011;14:758–64.
Dini-Andreote F, Stegen JC, van Elsas JD, Salles JF. Disentangling mechanisms that mediate the balance between stochastic and deterministic processes in microbial succession. Proc Natl Acad Sci USA. 2015;112:E1326–32.
Fierer N, Nemergut D, Knight R, Craine JM. Changes through time: integrating microorganisms into the study of succession. Res Microbiol. 2010;161:635–42.
Jackson CR. Changes in community properties during microbial succession. Oikos. 2003;2:444–8.
Del Moral R, Bliss LC. Mechanisms of primary succession: insights resulting from the eruption of Mount St Helens. Adv Ecol Res. 1993;24:1–66.
Read QD, Moorhead LC, Swenson NG, Bailey JK, Sanders NJ. Convergent effects of elevation on functional leaf traits within and among species. Funct Ecol. 2014;28:37–45.
Goberna M, Navarro-Cano JA, Valiente-Banuet A, García C, Verdú M. Abiotic stress tolerance and competition-related traits underlie phylogenetic clustering in soil bacterial communities. Ecol Lett. 2014;17:1191–201.
Garnier E, Cortez J, Billès G, Navas ML, Roumet C, Debussche M, et al. Plant functional markers capture ecosystem properties during secondary succession. Ecology. 2004;85:2630–7.
Fukami T, Martijn Bezemer T, Mortimer SR, Putten WH. Species divergence and trait convergence in experimental plant community assembly. Ecol Lett. 2005;8:1283–90.
McGill BJ, Enquist BJ, Weiher E, Westoby M. Rebuilding community ecology from functional traits. Trends Ecol Evol. 2006;21:178–85.
Burke C, Steinberg P, Rusch DB, Kjelleberg S, Thomas T. Bacterial community assembly based on functional genes rather than species. Proc Natl Acad Sci USA. 2011;108:14288–93.
Klappenbach JA, Dunbar JM, Thomas M, Schmidt TM. rRNA operon copy number reflects ecological strategies of bacteria. Appl Envir Microbiol. 2000;66:1328–33.
Nemergut DR, Knelman JE, Ferrenberg S, Bilinski T, Melbourne B, Jiang L, et al. Decreases in average bacterial community rRNA operon copy number during succession. ISME J. 2015;10:1147–56.
Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics. 2014;30:2114–20.
Wattam AR, Abraham D, Dalay O, Disz TL, Driscoll T, Gabbard JL, et al. PATRIC, the bacterial bioinformatics database and analysis resource. Nucleic Acids Res. 2014;42:581–91.
Markowitz VM, Chen I-MA, Palaniappan K, Chu K, Szeto E, Pillay M, et al. IMG 4 version of the integrated microbial genomes comparative analysis system. Nucleic Acids Res. 2014;42:D560–7.
Edgar RC. Search and clustering orders of magnitude faster than BLAST. Bioinformatics. 2010;26:2460–1.
Barberán A, Ramirez KS, Leff JW, Bradford MA, Wall DH, Fierer N. Why are some microbes more ubiquitous than others? Predicting the habitat breadth of soil bacteria. Ecol Lett. 2014;17:794–802.
Zhou J, He Z, Yang Y, Deng Y, Tringe SG, Alvarez-cohen L. High-throughput metagenomic technologies for complex microbial community analysis: open and closed formats. MBio. 2015;6:e02288–14.
Langille MGI, Zaneveld J, Caporaso JG, McDonald D, Knights D, Reyes Ja, et al. Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nat Biotechnol. 2013;31:814–21.
Zhang Y, Lin K. A phylogenomic analysis of Escherichia coli/Shigella group: implications of genomic features associated with pathogenicity and ecological adaptation. BMC Evol Biol. 2012;12:174.
Ortiz-Álvarez R, de los Ríos A, Fernández-Mendoza F, Torralba-Burrial A, Pérez-Ortega S. Ecological specialization of two photobiont-specific maritime cyanolichen species of the genus Lichina. PLoS ONE. 2015;10:e0132718.
McMurdie PJ, Holmes S. Waste not, want not: why rarefying microbiome data is inadmissible. PLoS Comput Biol. 2014;10:e1003531.
Hugenholtz P, Goebel B, Pace N. Impact of culture-independent studies on the emerging phylogenetic view of bacterial diversity. J Bacteriol. 1998;180:4765–74.
Auguet J-C, Barberan A, Casamayor EO. Global ecological patterns in uncultured Archaea. ISME J. 2010;4:182–90.
Lozupone Ca, Knight R. Global patterns in bacterial diversity. Proc Natl Acad Sci USA. 2007;104:11436–40.
McKenney Ea, Rodrigo A, Yoder AD. Patterns of gut bacterial colonization in three primate species. PLoS ONE. 2015;10:e0124618.
Costello E, Carlisle E, Bik E, Morowitz MJ, Relman DA. Microbiome assembly across multiple body sites in low-birthweight infants. MBio. 2013;4:e00782-13.
La Rosa PS, Warner BB, Zhou Y, Weinstock GM, Sodergren E, Hall-Moore CM, et al. Patterned progression of bacterial populations in the premature infant gut. Proc Natl Acad Sci USA. 2014;111:12522–7.
Vallès Y, Artacho A, Pascual-García A, Ferrús ML, Gosalbes MJ, Abellán JJ, et al. Microbial succession in the gut: directional trends of taxonomic and functional change in a birth cohort of Spanish infants. PLoS Genet. 2014;10:e1004406.
Moran NA, Wernegreen JJ. Lifestyle evolution in symbiotic bacteria: insights from genomics. Trends Ecol Evol. 2000;15:321–6.
Allison SD, Martiny JBH. Colloquium paper: resistance, resilience, and redundancy in microbial communities. Proc Natl Acad Sci USA. 2008;105:11512–9.
Burns AR, Stephens WZ, Stagaman K, Wong S, Rawls JF, Guillemin K, et al. Contribution of neutral processes to the assembly of gut microbial communities in the zebrafish over host development. ISME J. 2016;10:655–64.
Chase JM. Community assembly: when should history matter? Oecologia. 2003;136:489–98.
Peter H, Hörtnagl P, Reche I, Sommaruga R. Bacterial diversity and composition during rain events with and without Saharan dust influence reaching a high mountain lake in the Alps. Environ Microbiol Rep. 2014;6:618–24.
Ruiz-González C, Niño-García JP, del Giorgio PA. Terrestrial origin of bacterial communities in complex boreal freshwater networks. Ecol Lett. 2015;18:1198–206.
Margalef R. On certain unifying principles in ecology. Am Nat. 1963;97:357.
Franzenburg S, Fraune S, Altrock PM, Künzel S, Baines JF, Traulsen A, et al. Bacterial colonization of Hydra hatchlings follows a robust temporal pattern. ISME J. 2013;7:781–90.
Casamayor EO, Triadó-Margarit X, Castañeda C. Microbial biodiversity in saline shallow lakes of the Monegros Desert, Spain. FEMS Microbiol Ecol. 2013;85:503–18.
Casamayor EO, Massana R, Benlloch S, Øvreås L, Díez B, Goddard VJ, et al. Changes in archaeal, bacterial and eukaryal assemblages along a salinity gradient by comparison of genetic fingerprinting methods in a multipond solar saltern. Environ Microbiol. 2002;4:338–48.
Jackson CR, Churchill PF, Roden EE. Successional changes in bacterial assemblage structure during epilithic biofilm development. Ecology. 2001;82:555–66.
Fukami T. Historical contingency in community assembly: integrating niches, species pools, and priority effects. Annu Rev Ecol Evol Syst. 2015;46:1–23.
Vellend M. Conceptual synthesis in community ecology. Q Rev Biol. 2010;85:183–206.
Konstantinidis KT, Tiedje JM. Trends between gene content and genome size in prokaryotic species with larger genomes. Proc Natl Acad Sci USA. 2004;101:3160–5.
Leff JW, Jones SE, Prober SM, Barberán A, Borer ET, Firn JL, et al. Consistent responses of soil microbial communities to elevated nutrient inputs in grasslands across the globe. Proc Natl Acad Sci USA. 2015;112:10967–72.
Foerstner KU, von Mering C, Hooper SD, Bork P. Environments shape the nucleotide composition of genomes. EMBO Rep. 2005;6:1208–13.
Barberán A, Fernández-Guerra A, Bohannan BJM, Casamayor EO. Exploration of community traits as ecological markers in microbial metagenomes. Mol Ecol. 2012;21:1909–17.
Garcia JaL, Fernández-Guerra A, Casamayor EO. A close relationship between primary nucleotides sequence structure and the composition of functional genes in the genome of prokaryotes. Mol Phylogenet Evol. 2011;61:650–8.
Knelman JE, Schmidt SK, Lynch RC, Darcy JL, Castle SC, Cleveland CC, et al. Nutrient addition dramatically accelerates microbial community succession. PLoS ONE. 2014;9:e102609.
Correll DL. Phosphorus: a rate limiting nutrient in surface waters. Poult Sci. 1999;78:674–82.
Schmidt SK, Cleveland CC, Nemergut DR, Reed SC, King AJ, Sowell P. Estimating phosphorus availability for microbial growth in an emerging landscape. Geoderma. 2011;163:135–40.
Brasell Ka, Heath MW, Ryan KG, Wood Sa. Successional change in microbial communities of benthic Phormidium-dominated biofilms. Microb Ecol. 2015;69:254–66.
Thingstad TF, Skjoldal EF, Bohne RA. Phosphorus cycling and algal-bacterial competition in Sandsfjord, western Norway. Mar Ecol Prog Ser. 1993;99:239–59.
Richardson AE, Simpson RJ. Soil microorganisms mediating phosphorus availability update on microbial phosphorus. Plant Physiol. 2011;156:989–96.
Vila-Costa M, Sharma S, Moran MA, Casamayor EO. Diel gene expression profiles of a phosphorus limited mountain lake using metatranscriptomics. Environ Microbiol. 2013;15:1190–203.
Zubkov MV, Mary I, Woodward EMS, Warwick PE, Fuchs BM, Scanlan DJ, et al. Microbial control of phosphate in the nutrient-depleted North Atlantic subtropical gyre. Environ Microbiol. 2007;9:2079–89.
Clements FE. Plant succession: an analysis of the development of vegetation. Washington, DC: Carnegie Institution of Washington; 1916.
Prach K, Walker LR. Four opportunities for studies of ecological succession. Trends Ecol Evol. 2011;26:119–23.
Garbeva P, van Veen Ja, van Elsas JD. Microbial diversity in soil: selection microbial populations by plant and soil type and implications for disease suppressiveness. Annu Rev Phytopathol. 2004;42:243–70.
Buffie CG, Pamer EG. Microbiota-mediated colonization resistance against intestinal pathogens. Nat Rev Immunol. 2013;13:790–801.
Rockström J, Steffen W, Noone K, Persson Å, Chapin FS, Lambin E et al. Planetary boundaries: exploring the safe operating space for humanity. Ecol Soc. 2009;14. e-pub ahead of print https://doi.org/10.1038/461472a.
Plassart P, Akpa Vinceslas M, Gangneux C, Mercier A, Barray S, Laval K. Molecular and functional responses of soil microbial communities under grassland restoration. Agric Ecosyst Environ. 2008;127:286–93.
Acknowledgements
This work would not have been possible without the original articles that studied ecological succession. We thank all the authors from the original articles; especially we thank S Pérez-Ortega and MA Fernández-Martínez for their valuable feedback and sampling of glacial chronosequences (C4), and Xavier Triadó-Margarit for sampling of D2-D4 in Monegros. ROA was supported through the Spanish FPI PhD scholarships program (MINECO). Funding was provided by grants BRIDGES, CGL2015-69043-P (ROA and EOC), and CTM2015-64728-C2-2-R (AR) from the Spanish Office of Science (MINECO).
Author information
Authors and Affiliations
Corresponding authors
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Rights and permissions
About this article
Cite this article
Ortiz-Álvarez, R., Fierer, N., de los Ríos, A. et al. Consistent changes in the taxonomic structure and functional attributes of bacterial communities during primary succession. ISME J 12, 1658–1667 (2018). https://doi.org/10.1038/s41396-018-0076-2
Received:
Revised:
Accepted:
Published:
Issue date:
DOI: https://doi.org/10.1038/s41396-018-0076-2
This article is cited by
-
Random mechanisms govern bacterial succession in bioinoculated beet plants
Scientific Reports (2025)
-
Hurricane Otto’s influence on a tropical forests soil carbon, nitrogen, decomposition, and decomposer microbial communities over 5 years
Soil Ecology Letters (2025)
-
Dual-Domain Primary Succession of Bacteria in Glacier Forefield Streams and Soils of a Maritime and Continental Glacier
Microbial Ecology (2025)
-
Acidification associated with plant phosphorus-acquisition strategies decreases nutrient cycling potential of rhizosphere bacteria along the Hailuogou post-glacial chronosequence
Plant and Soil (2025)
-
Divergent maturational patterns of the infant bacterial and fungal gut microbiome in the first year of life are associated with inter-kingdom community dynamics and infant nutrition
Microbiome (2024)