Biological Sciences Division
Published September 3, 2019 | Version v1
Journal article Open

Single-amino acid variants reveal evolutionary processes that shape the biogeography of a global SAR11 subclade

Creators

  • 1. University of Chicago
  • 2. University of South Florida
  • 3. University of Hawaii at Manoa
  • 4. Oregon State University

Description

Members of the SAR11 order Pelagibacterales dominate the surface oceans. Their extensive diversity challenges emerging operational boundaries defined for microbial 'species' and complicates efforts of population genetics to study their evolution. Here, we employed single-amino acid variants (SAAVs) to investigate ecological and evolutionary forces that maintain the genomic heterogeneity within ubiquitous SAR11 populations we accessed through metagenomic read recruitment using a single isolate genome. Integrating amino acid and protein biochemistry with metagenomics revealed that systematic purifying selection against deleterious variants governs non-synonymous variation among very closely related populations of SAR11. SAAVs partitioned metagenomes into two main groups matching large-scale oceanic current temperatures, and six finer proteotypes that connect distant oceanic regions. These findings suggest that environmentally-mediated selection plays a critical role in the journey of cosmopolitan surface ocean microbial populations, and the idea 'everything is everywhere but the environment selects' has credence even at the finest resolutions.

Data availability

The vast majority of analyses relied on the open-source software platform anvi'o v2.4.0 (available from http://merenlab.org/software/anvio). The URL http://merenlab.org/data/sar11-saavs serves the remaining custom code used in our analyses. We made available (1) SAR11 isolate genomes (doi:10.6084/m9.figshare.5248945), (2) the anvi'o contigs database and merged profile for SAR11 genomes across metagenomes (doi:10.5281/zenodo.835218) and the static HTML summary for the mapping results (doi:10.6084/m9.figshare.5248453), (3) the SAR11 metapangenome (doi:10.6084/m9.figshare.5248459), single-nucleotide and single-amino acid variant reports for 1a.3.V across 74 TARA Oceans metagenomes (doi:10.6084/m9.figshare.5248447), and (4) SAAVs overlaid on predicted tertiary structures of 58 core 1a.3.V genes (doi:10.6084/m9.figshare.5248432). The URL http://anvi-server.org/p/4Q2TNo serves an interactive version of the SAR11 metapangenome, and the URL http://data.merenlab.org/sar11-saavs serves an interactive web page to investigate the link between SAAVs and predicted protein structures.

The following data sets were generated:

A Murat Eren (2017) figshare Anvi'o split profile for HIMB83 across metagenomes. https://doi.org/10.6084/m9.figshare.5248435

A Murat Eren (2017) figshare The SAR11 Metapangenome. https://doi.org/10.6084/m9.figshare.5248459

A Murat Eren (2017) figshare Anvi'o summary of SAR11 genomes across metagenomes. https://doi.org/10.6084/m9.figshare.5248453

A Murat Eren (2017) figshare Raw SNV and SAAV data for SAR11 1a.3.V. https://doi.org/10.6084/m9.figshare.5248447

A Murat Eren (2017) figshare S-LLPA SAAVs. https://doi.org/10.6084/m9.figshare.5248432

A Murat Eren (2017) Zenodo Anvi'o merged profile database for 21 SAR11 isolates across metagenomes. https://doi.org/10.5281/zenodo.835218

The following previously published data sets were used:

Shinichi Sunagawa et al. (2015) NCBI SRA ID PRJEB1787. Ocean plankton. Structure and function of the global ocean microbiome. https://www.ncbi.nlm.nih.gov/sra/?term=PRJEB1787

Anna Kopf et al. (2015) EMBL-EBI ID PRJEB5129. The ocean sampling day consortium. https://www.ebi.ac.uk/ena/data/view/PRJEB5129

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Additional details

Identifiers

DOI
10.7554/eLife.46497
Other
oai:uchicago.tind.io:9928

Funding

University of Chicago
Marine Biological Laboratory

UChicago Information

Division(s)
Biological Sciences Division
Department(s)
Biophysical Sciences, Medicine