Bacterial Degradation of Phosphonates Bound to High-Molecular-Weight Dissolved Organic Matter Produces Methane and Other Hydrocarbons

The biological degradation of dissolved organic matter (DOM) plays important roles in the carbon cycle and energy balance of the ocean. Yet, the biochemical pathways that drive DOM turnover remain to be fully characterized. In this study, we tested the ability of two open ocean bacterial isolates (a Pseudomonas stutzeri strain (Gammaproteobacteria) and a Sulfitobacter isolate (Alphaproteobacteria)) to degrade DOM phosphonates. Each isolate encoded a complete phosphonate degradation pathway in its genome, and each was able to degrade simple alkyl-phosphonates like methyl phosphonate, releasing methane (or other short chain hydrocarbon gases) as a result. We found that cultures incubated in the presence of HMW DOM polysaccharides also produced methane and other trace gases under aerobic conditions. To demonstrate that phosphonates were the source of these gases, we constructed a P. stutzeri mutant disabled in the phosphonate degradation pathway. Unlike the wild type, the mutant strain was deficient in the production of methane and other gases from HMW DOM-associated phosphonates. These observations support the hypothesis that DOM-bound methyl phosphonates may be a significant source of methane in the water column, and that bacterial degradation of these compounds likely contribute to the subsurface methane maxima observed throughout the world’s oceans.