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Abstract In oligotrophic ocean regions, dissolved organic phosphorus (DOP) plays a prominent role as a source of phosphorus (P) to microorganisms. An important bioavailable component of DOP is phosphonates, organophosphorus compounds with a carbon‐phosphorus (C‐P) bond, which are ubiquitous in high molecular weight dissolved organic matter (HMWDOM). In addition to being a source of P, the degradation of phosphonates by the bacterial C‐P lyase enzymatic pathway causes the release of trace hydrocarbon gases relevant to climate and atmospheric chemistry. In this study, we investigated the roles of phosphate and phosphonate cycling in the production of methane (CH4) and ethylene (C2H4) in the western North Atlantic Ocean, a region that features a transition in phosphate concentrations from coastal to open ocean waters. We observed an inverse relationship between phosphate and the saturation state of CH4and C2H4in the water column, and between phosphate and the relative abundance of the C‐P lyase marker genephnJ. In phosphate‐depleted waters, methylphosphonate and 2‐hydroxyethylphosphonate, the C‐P lyase substrates that yield CH4and C2H4, respectively, were readily degraded in proportions consistent with their abundance and bioavailability in HMWDOM and with the concentrations of CH4and C2H4in the water column. We conclude that phosphonate degradation through the C‐P lyase pathway is an important source and a common production pathway of CH4and C2H4in the phosphate‐depleted surface waters of the western North Atlantic Ocean and that phosphate concentration can be an important control on the saturation state of these gases in the upper ocean.
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Phosphate‐limited ocean regions select for bacterial populations enriched in the carbon–phosphorus lyase pathway for phosphonate degradation
Summary In tropical and subtropical oceanic surface waters phosphate scarcity can limit microbial productivity. However, these environments also have bioavailable forms of phosphorus incorporated into dissolved organic matter (DOM) that microbes with the necessary transport and hydrolysis metabolic pathways can access to supplement their phosphorus requirements. In this study we evaluated how the environment shapes the abundance and taxonomic distribution of the bacterial carbon–phosphorus (C–P) lyase pathway, an enzyme complex evolved to extract phosphate from phosphonates. Phosphonates are organophosphorus compounds characterized by a highly stable C–P bond and are enriched in marine DOM. Similar to other known bacterial adaptions to low phosphate environments, C–P lyase was found to become more prevalent as phosphate concentrations decreased. C–P lyase was particularly enriched in the Mediterranean Sea and North Atlantic Ocean, two regions that feature sustained periods of phosphate depletion. In these regions, C–P lyase was prevalent in several lineages ofAlphaproteobacteria(Pelagibacter, SAR116,RoseobacterandRhodospirillales),Gammaproteobacteria,andActinobacteria. The global scope of this analysis supports previous studies that infer phosphonate catabolism via C–P lyase is an important adaptive strategy implemented by bacteria to alleviate phosphate limitation and expands the known geographic extent and taxonomic affiliation of this metabolic pathway in the ocean.
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- Award ID(s):
- 1756517
- PAR ID:
- 10461282
- Publisher / Repository:
- Wiley-Blackwell
- Date Published:
- Journal Name:
- Environmental Microbiology
- Volume:
- 21
- Issue:
- 7
- ISSN:
- 1462-2912
- Format(s):
- Medium: X Size: p. 2402-2414
- Size(s):
- p. 2402-2414
- Sponsoring Org:
- National Science Foundation
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