Abstract
SAR86 is an abundant and ubiquitous heterotroph in the surface ocean that plays a central role in the function of marine ecosystems. We hypothesized that despite its ubiquity, different SAR86 subgroups may be endemic to specific ocean regions and functionally specialized for unique marine environments. However, the global biogeographical distributions of SAR86 genes, and the manner in which these distributions correlate with marine environments, have not been investigated. We quantified SAR86 gene content across globally distributed metagenomic samples and modeled these gene distributions as a function of 51 environmental variables. We identified five distinct clusters of genes within the SAR86 pangenome, each with a unique geographic distribution associated with specific environmental characteristics. Gene clusters are characterized by the strong taxonomic enrichment of distinct SAR86 genomes and partial assemblies, as well as differential enrichment of certain functional groups, suggesting differing functional and ecological roles of SAR86 ecotypes. We then leveraged our models and high-resolution, remote sensing-derived environmental data to predict the distributions of SAR86 gene clusters across the world’s oceans, creating global maps of SAR86 ecotype distributions. Our results reveal that SAR86 exhibits previously unknown, complex biogeography, and provide a framework for exploring geographic distributions of genetic diversity from other microbial clades.
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
Falkowski PG, Fenchel T, Delong EF. The microbial engines that drive Earth’s biogeochemical cycles. Science. 2008;320:1034–9.
Azam F. Microbial control of oceanic carbon flux: The plot thickens. Science. 1998;280:694–6.
Shi Y, Tyson GW, Eppley JM, Delong EF. Integrated metatranscriptomic and metagenomic analyses of stratified microbial assemblages in the open ocean. ISME J. 2011;5:999–1013.
Delong EF, Preston CM, Mincer T, Rich V, Hallam SJ, Frigaard N, et al. Community genomics among stratified microbial assemblages in the ocean’s interior. Science. 2006;311:496–503.
Raes J, Letunic I, Yamada T, Jensen LJ, Bork P. Toward molecular trait-based ecology through integration of biogeochemical, geographical and metagenomic data. Mol Syst Biol. 2011;7:473.
Guidi L, Chaffron S, Bittner L, Eveillard D, Larhlimi A, Roux S, et al. Plankton networks driving carbon export in the oligotrophic ocean. Nature. 2016;532:465–70.
Morales SE, Holben WE. Linking bacterial identities and ecosystem processes: can ‘omic’ analyses be more than the sum of their parts? FEMS Microbiol Ecol. 2011;75:2–16.
Louca S, Parfrey LW, Doebeli M. Decoupling function and taxonomy in the global ocean microbiome. Science. 2016;353:1272–7.
Sunagawa S, Coelho LP, Chaffron S, Kultima JR, Labadie K, Salazar G, et al. Structure and function of the global ocean microbiome. Science. 2015;348:1–10.
Widder S, Allen RJ, Pfeiffer T, Curtis TP, Wiuf C, Sloan WT, et al. Challenges in microbial ecology: building predictive understanding of community function and dynamics. ISME J. 2016;10:2557–68.
Treseder KK, Balser TC, Bradford MA, Brodie EL, Dubinsky EA, Eviner VT, et al. Integrating microbial ecology into ecosystem models: Challenges and priorities. Biogeochemistry. 2012;109:7–18.
Wieder WR, Allison SD, Davidson EA, Georgiou K, Hararuk O, He Y, et al. Explicitly representing soil microbial processes in Earth system models. Glob Biogeochem Cycles. 2015;29:1782–1800.
Cohan FM. Towards a conceptual and operational union of bacterial systematics, ecology, and evolution. Philos Trans R Soc B Biol Sci. 2006;361:1985–96.
Begon M, Townsend C, Harper J. Ecology: from individuals to ecosystems, 4th ed. Oxford, UK: Blackwell Publishing; 2006.
Carlson CA, Morris R, Parsons R, Treusch AH, Giovannoni SJ, Vergin K. Seasonal dynamics of SAR11 populations in the euphotic and mesopelagic zones of the northwestern Sargasso Sea. ISME J. 2009;3:283–95.
Martiny JBH, Bohannan BJM, Brown JH, Colwell RK, Fuhrman JA, Green JL, et al. Microbial biogeography: putting microorganisms on the map. Nat Rev Microbiol. 2006;4:102–12.
Ladau J, Sharpton TJ, Finucane MM, Jospin G, Kembel SW, O’Dwyer J, et al. Global marine bacterial diversity peaks at high latitudes in winter. ISME J. 2013;7:1669–77.
Zinger L, Amaral-Zettler La, Fuhrman JA, Horner-Devine MC, Huse S, Welch DBM, et al. Global patterns of bacterial beta-diversity in seafloor and seawater ecosystems. PLoS ONE. 2011;6:e24570.
Jiang X, Langille MGI, Neches RY, Elliot M, Levin Sa, Eisen Ja, et al. Functional biogeography of ocean microbes revealed through non-negative matrix factorization. PLoS ONE. 2012;7:1–9.
Nayfach S, Rodriguez-Mueller B, Garud N, Pollard KS. An integrated metagenomics pipeline for strain profiling reveals novel patterns of bacterial transmission and biogeography. Genome Res. 2016;26:1612–25.
Kent AG, Dupont CL, Yooseph S, Martiny AC. Global biogeography of Prochlorococcus genome diversity in the surface ocean. ISME J. 2016;10:1856–65.
Britschgi TB, Giovannoni SJ. Phylogenetic analysis of a natural marine bacterioplankton population by rRNA gene cloning and sequencing. Appl Environ Microbiol. 1991;57:1707–13.
Suzuki MT, Beja O, Taylor LT, Delong EF. Phylogenetic analysis of ribosomal RNA operons from uncultivated coastal marine bacterioplankton. Environ Microbiol. 2001;3:323–31.
Treusch AH, Vergin KL, Finlay LA, Donatz MG, Burton RM, Carlson CA, et al. Seasonality and vertical structure of microbial communities in an ocean gyre. ISME J. 2009;3:1148–63.
Dupont CL, Rusch DB, Yooseph S, Lombardo MJ, Alexander Richter R, Valas R, et al. Genomic insights to SAR86, an abundant and uncultivated marine bacterial lineage. ISME J. 2012;6:1186–99.
Rusch DB, Lombardo M-J, Yee-Greenbaum J, Novotny M, Brinkac LM, Lasken RS, et al. Draft genome sequence of a single cell of SAR86 clade subgroup IIIa. Genome Announc. 2013;1:e00030–12.
Swan BK, Tupper B, Sczyrba A, Lauro FM, Martinez-Garcia M, González JM, et al. Prevalent genome streamlining and latitudinal divergence of planktonic bacteria in the surface ocean. Proc Natl Acad Sci USA. 2013;110:11463–8.
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.
Hoarfrost A. SAR86. Github repository. Zenodo. https://doi.org/10.5281/zenodo.1476732.
Finn RD, Coggill P, Eberhardt RY, Eddy SR, Mistry J, Mitchell AL, et al. The Pfam protein families database: towards a more sustainable future. Nucleic Acids Res. 2016;44:D279–85.
Béjà O, Aravind L, Koonin EV, Suzuki MT, Hadd A, Nguyen LP. et al. Bacterial rhodopsin: evidence for a new type of phototrophy in the sea. Science. 2017;289:1902–6.
Lombard V, Golaconda Ramulu H, Drula E, Coutinho PM, Henrissat B. The carbohydrate-active enzymes database (CAZy) in 2013. Nucleic Acids Res. 2014;42:490–5.
Sabehi G, Béjà O, Suzuki MT, Preston CM, DeLong EF. Different SAR86 subgroups harbour divergent proteorhodopsins. Environ Microbiol. 2004;6:903–10.
Béja O, Spudich EN, Spudich JL, Leclerc M, DeLong EF. Proteorhodopsin phototrophy in the ocean. Nature. 2001;411:786–9.
Aguilar D, Aviles FX, Querol E, Sternberg MJE. Analysis of phenetic trees based on metabolic capabilites across the three domains of life. J Mol Biol. 2004;340:491–512.
Pommier T, Canbäck B, Riemann L, Boström KH, Simu K, Lundberg P, et al. Global patterns of diversity and community structure in marine bacterioplankton. Mol Ecol. 2007;16:867–80.
Galand PE, Pereira O, Hochart C, Auguet JC, Debroas D. A strong link between marine microbial community composition and function challenges the idea of functional redundancy. ISME J. 2018;12:2470–8.
Strickland MS, Lauber C, Fierer N, Bradford MA. Testing the functional significance of microbial community composition. Ecology. 2009;90:441–51.
Louca S, Polz MF, Mazel F, Albright MBN, Huber JA, O’Connor MI, et al. Function and functional redundancy in microbial systems. Nat Ecol Evol. 2018;2:936–43.
Louca S, Jacques SMS, Pires APF, Leal JS, Srivastava DS, Parfrey LW, et al. High taxonomic variability despite stable functional structure across microbial communities. Nat Ecol Evol. 2016;1:0015.
Martiny JBH, Jones SE, Lennon JT, Martiny AC. Microbiomes in light of traits: a phylogenetic perspective. Science (80-). 2015;350:aac9323.
Hunt DE, David LA, Gevers D, Preheim SP, Alm EJ, Polz MF. Resource partitioning and sympatric differentiation among closely related bacterioplanktn. Science. 2008;320:1081–5.
Noinaj N, Guiller M, Barnard TJ, Buchanan SK. TonB-dependent transporters: regulation, structure, and function. Annu Rev Microbiol. 2010;64:43–60.
Acknowledgements
This work was supported by a Deep Carbon Observatory Deep Life Modeling and Visualization Fellowship to AH; OCE-1736772 and DE-SC0013887 to CA; Gordon and Betty Moore Foundation grant #3300 to KSP; and grants from the Beyster Family Fund of the San Diego Foundation and Life Technologies Foundation to JCVI.
Author information
Authors and Affiliations
Contributions
CD and SY created the SAR86 co-assembly of SAR86 genes from the Global Ocean Sampling sequences, and CD annotated the SAR86 pangenome. SN created the pangenome and mapped TARA samples to the SAR86 pangenome. AH gathered satellite environmental data, created the models, did clustering, identified ecotypes, and analyzed data. JL gathered historical environmental data. All authors contributed to discussion of data and writing of the manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary information
Rights and permissions
About this article
Cite this article
Hoarfrost, A., Nayfach, S., Ladau, J. et al. Global ecotypes in the ubiquitous marine clade SAR86. ISME J 14, 178–188 (2020). https://doi.org/10.1038/s41396-019-0516-7
Received:
Revised:
Accepted:
Published:
Version of record:
Issue date:
DOI: https://doi.org/10.1038/s41396-019-0516-7
This article is cited by
-
Genomic insights into cryptic cycles of microbial hydrocarbon production and degradation in contiguous freshwater and marine microbiomes
Microbiome (2023)
-
Atlantic water influx and sea-ice cover drive taxonomic and functional shifts in Arctic marine bacterial communities
The ISME Journal (2023)
-
Short-term acidification promotes diverse iron acquisition and conservation mechanisms in upwelling-associated phytoplankton
Nature Communications (2023)
-
Temporal variation in the prokaryotic community of a nearshore marine environment
Scientific Reports (2022)
-
Bacterioneuston and Bacterioplankton Structure and Abundance in Two Trophically Distinct Marine Environments — a Marine Lake and the Adjacent Coastal Site on the Adriatic Sea
Microbial Ecology (2022)
