Enrichment of polyphenol metabolism within the ubiquitous SAR116 ‘Puniceispirillales’ bacterioplankton

Abstract

Marine dissolved organic matter (DOM) is a complex pool of substrates, and a central challenge in marine biogeochemistry is to determine which DOM compounds are produced, consumed, or exchanged by microorganisms. Aromatic compounds, including polyphenols, comprise an important chemical class of marine DOM generated both in situ and also supplied via atmospheric deposition, terrestrial runoff, or natural seeps. Here we demonstrate, through pangenomics and metabolic reconstruction, the enrichment of genes for degradation of a wide variety of polyphenols in the cosmopolitan SAR116 bacterioplankton (Puniceispirillales). Gene and pathway conservation, the evolutionary history of key ring-cleaving dioxygenases, and expression patterns from global ocean surveys support the conclusion that these transformations represent core elements of SAR116 ecophysiology. The degradation pathway for protocatechuate, an end member for many polyphenol transformations, occurred in all subclades, and we found evidence of different evolutionary histories for genes in this pathway, including gene loss, analogous substitution, and retention of horizontally transferred genes from the Gammaproteobacteria. Furthermore, variation in these and other pathway-specific gene losses suggest that some SAR116 polyphenol metabolism may occur through a division of labor in concert with other community members and/or require novel or promiscuous enzymes. The enrichment and expression of polyphenol degradation pathways define a previously underappreciated metabolic niche for SAR116 and provides new evidence emphasizing the importance of polyphenol metabolism in the marine carbon cycle.