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Isolation and Characterization of Bacteria That Degrade Phosphonates in Marine Dissolved Organic Matter.

ABSTRACT: Semi-labile dissolved organic matter (DOM) accumulates in surface waters of the oligotrophic ocean gyres and turns over on seasonal to annual timescales. This reservoir of DOM represents an important source of carbon, energy, and nutrients to marine microbial communities but the identity of the microorganisms and the biochemical pathways underlying the cycling of DOM remain largely uncharacterized. In this study we describe bacteria isolated from the North Pacific Subtropical Gyre (NPSG) near Hawaii that are able to degrade phosphonates associated with high molecular weight dissolved organic matter (HMWDOM), which represents a large fraction of semi-labile DOM. We amended dilution-to-extinction cultures with HMWDOM collected from NPSG surface waters and with purified HMWDOM enriched with polysaccharides bearing alkylphosphonate esters. The HMWDOM-amended cultures were enriched in Roseobacter isolates closely related to Sulfitobacter and close relatives of hydrocarbon-degrading bacteria of the Oceanospirillaceae family, many of which encoded phosphonate degradation pathways. Sulfitobacter cultures encoding C-P lyase were able to catabolize methylphosphonate and 2-hydroxyethylphosphonate, as well as the esters of these phosphonates found in native HMWDOM polysaccharides to acquire phosphorus while producing methane and ethylene, respectively. Conversely, growth of these isolates on HMWDOM polysaccharides as carbon source did not support robust increases in cell yields, suggesting that the constituent carbohydrates in HMWDOM were not readily available to these individual isolates. We postulate that the complete remineralization of HMWDOM polysaccharides requires more complex microbial inter-species interactions. The degradation of phosphonate esters and other common substitutions in marine polysaccharides may be key steps in the turnover of marine DOM.

SUBMITTER: Sosa OA

PROVIDER: S-EPMC5649143 | biostudies-literature | 2017

REPOSITORIES: biostudies-literature

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Isolation and Characterization of Bacteria That Degrade Phosphonates in Marine Dissolved Organic Matter.

Sosa Oscar A OA Repeta Daniel J DJ Ferrón Sara S Bryant Jessica A JA Mende Daniel R DR Karl David M DM DeLong Edward F EF

Frontiers in microbiology 20170926

Semi-labile dissolved organic matter (DOM) accumulates in surface waters of the oligotrophic ocean gyres and turns over on seasonal to annual timescales. This reservoir of DOM represents an important source of carbon, energy, and nutrients to marine microbial communities but the identity of the microorganisms and the biochemical pathways underlying the cycling of DOM remain largely uncharacterized. In this study we describe bacteria isolated from the North Pacific Subtropical Gyre (NPSG) near Ha ...[more]

PMID: 29085339

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Project description:Marine dissolved organic matter (DOM) is a complex mixture of chemical compounds. At 750 Pg C, it is one of the biggest pools of reduced carbon on Earth. It has been proposed that the diversity of DOM is responsible for its recalcitrance. We hypothesize that the chemodiversity of marine DOM is a reflection of the chemodiversity of bacterial exometabolomes. To test this, we incubated two model strains of the Roseobacter group; Phaeobacter inhibens and Dinoroseobacter shibae in pure culture using three different simple organic compounds as sole carbon sources (glutamate, glucose, and acetate and succinate for P. inhibens and D. shibae, respectively). The exometabolome of the model organisms was characterized using Fourier Transform Ion Cyclotron Resonance Mass Spectrometry (FT-ICR-MS) and ecological diversity measures. We detected thousands of molecular masses in the exometabolomes of P. inhibens and D. shibae (21,105 and 9,386, respectively), reflecting the capability of single bacterial strains to diversify simple organic compounds. The chemical composition of the exometabolomes changed with growth phase and also differed according to the strain incubated and the utilized substrate. We mimicked a higher diversity of substrates, bacterial species and heterogeneous growth (different growth phases) to approach the complexity of natural environments, by computationally creating combinations of detected exometabolomes. We compared the chemodiversity of these combinations, indicative for chemodiversity of freshly produced microbial DOM to that of refractory DOM from one of the oldest oceanic water masses (North Equatorial Pacific Intermediate Water). Some combinations of exometabolomes showed higher richness than the deep ocean refractory DOM, and all the combinations showed higher functional diversity. About 15% of the 13,509 molecular formulae detected in exometabolomes and refractory oceanic DOM were shared, i.e., occurred in Roseobacter exometabolomes and in deep water samples. This overlap provides further support for our hypothesis that marine bacteria from the Roseobacter group contribute to the sustainability of marine DOM chemodiversity and stability.

Dataset Information

Isolation and Characterization of Bacteria That Degrade Phosphonates in Marine Dissolved Organic Matter.

Publications

Isolation and Characterization of Bacteria That Degrade Phosphonates in Marine Dissolved Organic Matter.

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