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 of
In the oligotrophic ocean where inorganic phosphate (Pi) concentrations are low, microorganisms supplement their nutrient requirements with phosphorus (P) extracted from dissolved organic matter (DOM). Most P in DOM is bound as phosphate esters, which are hydrolyzed by phosphoesterases to Pi. However, a large fraction of DOM‐P occurs as phosphonates, reduced organophosphorus compounds with a CP bond that do not yield Pithrough simple ester hydrolysis alone. Phosphonates require an additional step that cleaves the CP bond and oxidizes P(III) to P(V) to yield Pi. Most phosphonates are metabolized by the C‐P lyase pathway, which cleaves CP bonds and oxidizes phosphonates to Pi, enabling microbial assimilation. While the activity of common phosphoesterases such as alkaline phosphatase and phosphodiesterase can be measured by a fluorescent assay, a comparable method to assess C‐P lyase activity (CLA) in natural water samples does not exist. To address this, we synthesized a dansyl‐labeled phosphonate compound, and measured its hydrolysis by C‐P lyase using high performance liquid chromatography. We found that laboratory cultures of marine bacteria expressing the C‐P lyase pathway are able to hydrolyze the dansyl phosphonate, while bacteria expressing other phosphonate degradation pathways do not. Finally, we performed several field tests of the assay to measure water column profiles of CLA at Sta. ALOHA in the North Pacific Subtropical Gyre. Activity was elevated near the deep chlorophyll maximum suggesting high levels of phosphonate degradation in that region.
more » « less- Award ID(s):
- 1756517
- NSF-PAR ID:
- 10452733
- Publisher / Repository:
- Wiley Blackwell (John Wiley & Sons)
- Date Published:
- Journal Name:
- Limnology and Oceanography: Methods
- Volume:
- 19
- Issue:
- 4
- ISSN:
- 1541-5856
- Page Range / eLocation ID:
- p. 235-244
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Summary Alphaproteobacteria (Pelagibacter , SAR116,Roseobacter andRhodospirillales ),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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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 gene
phnJ . 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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