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Abstract The flux of carbon through the labile dissolved organic matter (DOM) pool supports marine microbial communities and represents the fate of approximately half of marine net primary production (NPP). However, the behavior of individual chemical structures that make up labile DOM remain largely unknown. We performed 12 uptake kinetics and two uptake competition experiments on the abundant betaine osmolytes glycine betaine (GBT) and homarine. Combining uptake kinetics with dissolved metabolite measurements, we quantified fluxes through the DOM pool. Fluxes were correlated with particulate concentrations and ranged from 0.53 to 41 and 0.003 to 0.54 nmol L⁻¹ d⁻¹for GBT and homarine, respectively, equivalent to up to 1.2% of NPP. Turnover times of dissolved GBT and homarine ranged from 1 to 57 d. Betaines and sulfoniums such as dimethylsulfoniopropionate competitively inhibited homarine uptake. Our results quantify GBT and homarine cycling and suggest an important role for uptake competition in regulating dissolved metabolite concentrations and fluxes. 

Abstract Homarine (N-methylpicolinic acid) is a ubiquitous marine metabolite produced by phytoplankton and noted for its bioactivity in marine animals, yet its microbial degradation pathways are uncharacterized. Here, we identify a conserved operon (homABCDER) that mediates homarine catabolism in bacteria using comparative transcriptomics, mutagenesis, and targeted knockouts. Phylogenetic and genomic analyses show this operon distributed across abundant bacterial clades, including coastal copiotrophs (e.g., Rhodobacterales) and open-ocean oligotrophs (e.g., SAR11, SAR116). High-resolution mass spectrometry revealed N-methylglutamic acid and glutamic acid as key metabolic products of homarine in both model and natural systems, with N-methylglutamate dehydrogenase catalyzing their conversion. Metatranscriptomics showed responsive and in situ expression of hom genes aligned with homarine availability. These findings uncover the genetic and metabolic basis of homarine degradation, establish its ecological relevance, and highlight homarine as a versatile growth substrate that feeds into central metabolism via glutamic acid in diverse marine bacteria. 

ABSTRACT The marine unicellular cyanobacterium Prochlorococcus is an abundant primary producer and widespread inhabitant of the photic layer in tropical and subtropical marine ecosystems, where the inorganic nutrients required for growth are limiting. In this study, we demonstrate that Prochlorococcus high-light strain MIT9301, an isolate from the phosphate-depleted subtropical North Atlantic Ocean, can oxidize methylphosphonate (MPn) and hydroxymethylphosphonate (HMPn), two phosphonate compounds present in marine dissolved organic matter, to obtain phosphorus. The oxidation of these phosphonates releases the methyl group as formate, which is both excreted and assimilated into purines in RNA and DNA. Genes encoding the predicted phosphonate oxidative pathway of MIT9301 were predominantly present in Prochlorococcus genomes from parts of the North Atlantic Ocean where phosphate availability is typically low, suggesting that phosphonate oxidation is an ecosystem-specific adaptation of some Prochlorococcus populations to cope with phosphate scarcity. IMPORTANCE Until recently, MPn was only known to be degraded in the environment by the bacterial carbon-phosphorus (CP) lyase pathway, a reaction that releases the greenhouse gas methane. The identification of a formate-yielding MPn oxidative pathway in the marine planctomycete Gimesia maris (S. R. Gama, M. Vogt, T. Kalina, K. Hupp, et al., ACS Chem Biol 14:735–741, 2019, https://doi.org/10.1021/acschembio.9b00024 ) and the presence of this pathway in Prochlorococcus indicate that this compound can follow an alternative fate in the environment while providing a valuable source of P to organisms. In the ocean, where MPn is a major component of dissolved organic matter, the oxidation of MPn to formate by Prochlorococcus may direct the flow of this one-carbon compound to carbon dioxide or assimilation into biomass, thus limiting the production of methane. 

Abstract In the oligotrophic ocean where inorganic phosphate (P_i) 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 P_i. However, a large fraction of DOM‐P occurs as phosphonates, reduced organophosphorus compounds with a CP bond that do not yield P_ithrough simple ester hydrolysis alone. Phosphonates require an additional step that cleaves the CP bond and oxidizes P(III) to P(V) to yield P_i. Most phosphonates are metabolized by the C‐P lyase pathway, which cleaves CP bonds and oxidizes phosphonates to P_i, 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. 

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.