Methane production by phosphate-starved SAR11 chemoheterotrophic marine bacteria

Abstract

The oxygenated surface waters of the world's oceans are supersaturated with methane relative to the atmosphere, a phenomenon termed the 'marine methane paradox'. The production of methylphosphonic acid (MPn) by marine archaea related to Nitrosopumilus maritimus and subsequent decomposition of MPn by phosphate-starved bacterioplankton may partially explain the excess methane in surface waters. Here we show that Pelagibacterales sp. strain HTCC7211, an isolate of the SAR11 clade of marine a-proteobacteria, produces methane from MPn, stoichiometric to phosphorus consumption, when starved for phosphate. Gene transcripts encoding phosphonate transport and hydrolysis proteins are upregulated under phosphate limitation, suggesting a genetic basis for the methanogenic phenotype. Strain HTCC7211 can also use 2-aminoethylphosphonate and assorted phosphate esters for phosphorus nutrition. Despite strain-specific differences in phosphorus utilization, these findings identify Pelagibacterales bacteria as a source of biogenic methane and further implicate phosphate starvation of chemoheterotrophic bacteria in the long-observed methane supersaturation in oxygenated waters.

SAR11 lipid renovation in response to phosphate starvation

“…HTCC7211 significantly induced the expression of 31 genes, including those encoding P i and organophosphorus transport and catabolism proteins (10). Proximal to the genes encoding a high-affinity P i transporter (pstSCAB), a four-gene cluster (HTCC7211_00011000-HTCC7211_00011030) was significantly up-regulated in P i starved cultures, relative to P i replete cultures (2.7-to 8.2-fold, reported in ref.…”

“…When P i limited, str. HTCC7211 induces a suite of these genes, including both inorganic (pstSCAB) and organophosphate (phnCDEE 2 ) ABC transporters and the C-P lyase complex (phnGHIJKLNM), required for phosphonate degradation (10). Laboratory experiments have distinctly linked the expression of these genes to the utilization of both phosphate esters and phosphonates (including methylphosphonate; MPn) (10).…”

“…HTCC7211 (str. HTCC7211) contains extended genetic inventory associated with P i acquisition, storage, and metabolism (10). When P i limited, str.…”

Oxic water column methanogenesis as a major component of aquatic CH4 fluxes

“…The presence 19,22,[26][27][28] and activity 19,22,27 of hydrogenotrophic and acetoclastic methanogenic archaea have been confirmed at the molecular level in diverse oxic environments. At the same time, marine studies suggest that the microbial decomposition of methylated compounds such as methanethiol 15 and methylphosphonate 16,[23][24][25] could be an important source of CH 4 in surface waters of the open ocean. Further, metalimnetic peaks of CH 4 are a recurrent feature in many ecosystems, which correlate positively with dissolved O 2 (DO), algal biomass and production [8][9][10]14,15,18,19 .…”

“…In vitro experiments point to CH 4 production in both microanoxic habitats in metazoan guts and on particles 14,[17][18][19][20][21][22][23] , and in particle-free oxic water 15,16,18,19,[23][24][25] , via multiple biochemical pathways. The presence 19,22,[26][27][28] and activity 19,22,27 of hydrogenotrophic and acetoclastic methanogenic archaea have been confirmed at the molecular level in diverse oxic environments.…”