Pangenomics analysis reveals diversification of enzyme families and niche specialization in globally abundant SAR202 bacteria
Saw, Jimmy H. W.
Kujawinski, Elizabeth B.
Carlson, Craig A.
Giovannoni, Stephen J.
MetadataShow full item record
KeywordSAR202; biological carbon pump; carbon sequestration; dissolved organic matter; enolase; marine carbon cycle; recalcitrant organic matter
It has been hypothesized that the abundant heterotrophic ocean bacterioplankton in the SAR202 clade of the phylum Chloroflexi evolved specialized metabolisms for the oxidation of organic compounds that are resistant to microbial degradation via common metabolic pathways. Expansions of paralogous enzymes were reported and implicated in hypothetical metabolism involving monooxygenase and dioxygenase enzymes. In the proposed metabolic schemes, the paralogs serve the purpose of diversifying the range of organic molecules that cells can utilize. To further explore SAR202 evolution and metabolism, we reconstructed single amplified genomes and metagenome-assembled genomes from locations around the world that included the deepest ocean trenches. In an analysis of 122 SAR202 genomes that included seven subclades spanning SAR202 diversity, we observed additional evidence of paralog expansions that correlated with evolutionary history, as well as further evidence of metabolic specialization. Consistent with previous reports, families of flavin-dependent monooxygenases were observed mainly in the group III SAR202 genomes, and expansions of dioxygenase enzymes were prevalent in those of group VII. We found that group I SAR202 genomes encode expansions of racemases in the enolase superfamily, which we propose evolved for the degradation of compounds that resist biological oxidation because of chiral complexity. Supporting the conclusion that the paralog expansions indicate metabolic specialization, fragment recruitment and fluorescent in situ hybridization (FISH) with phylogenetic probes showed that SAR202 subclades are indigenous to different ocean depths and geographical regions. Surprisingly, some of the subclades were abundant in surface waters and contained rhodopsin genes, altering our understanding of the ecological role of SAR202 species in stratified water columns. IMPORTANCE The oceans contain an estimated 662 Pg C in the form of dissolved organic matter (DOM). Information about microbial interactions with this vast resource is limited, despite broad recognition that DOM turnover has a major impact on the global carbon cycle. To explain patterns in the genomes of marine bacteria, we propose hypothetical metabolic pathways for the oxidation of organic molecules that are resistant to oxidation via common pathways. The hypothetical schemes we propose suggest new metabolic pathways and classes of compounds that could be important for understanding the distribution of organic carbon throughout the biosphere. These genome-based schemes will remain hypothetical until evidence from experimental cell biology can be gathered to test them. Our findings also fundamentally change our understanding of the ecology of SAR202 bacteria, showing that metabolically diverse variants of these cells occupy niches spanning all depths and are not relegated to the dark ocean.
© The Author(s), 2019. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Saw, J. H. W., Nunoura, T., Hirai, M., Takaki, Y., Parsons, R., Michelsen, M., Longnecker, K., Kujawinski, E. B., Stepanauskas, R., Landry, Z., Carlson, C. A., & Giovannoni, S. J. Pangenomics analysis reveals diversification of enzyme families and niche specialization in globally abundant SAR202 bacteria. Mbio, 11(1), (2020): e02975-19, doi:10.1128/mBio.02975-19.
Suggested CitationSaw, J. H. W., Nunoura, T., Hirai, M., Takaki, Y., Parsons, R., Michelsen, M., Longnecker, K., Kujawinski, E. B., Stepanauskas, R., Landry, Z., Carlson, C. A., & Giovannoni, S. J. (2020). Pangenomics analysis reveals diversification of enzyme families and niche specialization in globally abundant SAR202 bacteria. Mbio, 11(1), e02975-19.
The following license files are associated with this item:
Showing items related by title, author, creator and subject.
Concentrations of colored dissolved organic matter, dissolved organic carbon, and total phosphorous from experiments conducted at the University of Hawaii, Manoa in 2015 (Coral DOM2) Nelson, Craig E (Biological and Chemical Oceanography Data Management Office (BCO-DMO). Contact: firstname.lastname@example.org, 2019-06-27)Concentrations of colored dissolved organic matter, dissolved organic carbon, and total phosphorous from experiments conducted at the University of Hawaii, Manoa in 2015. For a complete list of measurements, refer to the ...
Role of iron and organic carbon in mass-specific light absorption by particulate matter from Louisiana coastal waters Estapa, Margaret L.; Boss, Emmanuel S.; Mayer, Lawrence M.; Roesler, Collin S. (Association for the Sciences of Limnology and Oceanography, 2012-01)We investigated the influences of organic content and mineralogical composition on light absorption by mostly mineral suspended particles in aquatic and coastal marine systems. Mass-specific absorption spectra of suspended ...
Impact of circulation on export production, dissolved organic matter, and dissolved oxygen in the ocean : results from Phase II of the Ocean Carbon-cycle Model Intercomparison Project (OCMIP-2) Najjar, Raymond G.; Jin, X.; Louanchi, F.; Aumont, Olivier; Caldeira, Ken; Doney, Scott C.; Dutay, J.-C.; Follows, Michael J.; Gruber, Nicolas; Joos, Fortunat; Lindsay, Keith; Maier-Reimer, Ernst; Matear, Richard J.; Matsumoto, K.; Monfray, Patrick; Mouchet, Anne; Orr, James C.; Plattner, Gian-Kasper; Sarmiento, Jorge L.; Schlitzer, Reiner; Slater, Richard D.; Weirig, Marie-France; Yamanaka, Yasuhiro; Yool, Andrew (American Geophysical Union, 2007-08-08)Results are presented of export production, dissolved organic matter (DOM) and dissolved oxygen simulated by 12 global ocean models participating in the second phase of the Ocean Carbon-cycle Model Intercomparison Project. ...