Synergistic metabolism of a broad range of C1 compounds in the marine methylotrophic bacterium HTCC2181

Abstract

The 1.3 Mbp genome of HTCC2181, a member of the abundant OM43 clade of coastal bacterioplankton, suggested it is an obligate methylotroph. Preliminary experiments demonstrated that methanol and formaldehyde, but not other common C1 compounds such as methylamine, could support growth. Methanol concentrations in seawater are reportedly < 100 nM, suggesting either that the flux of methanol through plankton pools is very rapid, or that methanol may not be the primary growth substrate for HTCC2181. Therefore, we investigated the apparent extreme substrate range restriction of HTCC2181 in greater detail. Growth rate and maximum cell density of HTCC2181 increased with methanol concentration, yielding a K(s) value of 19 µM. In contrast, no growth was observed in the presence of the methylated (C1) compounds, methyl chloride, trimethylamine-oxide (TMAO) or dimethylsulfoniopropionate (DMSP) when they were the sole substrates. However, growth rate, maximum cell density and cellular ATP content were significantly enhanced when any of these methylated compounds were provided in the presence of a limiting concentration of methanol. These observations fit a model in which the metabolic intermediate formaldehyde is required for net carbon assimilation, allowing C1 substrates that do not produce a formaldehyde intermediate to be oxidized for energy, but not assimilated into biomass. Rates of methanol and TMAO oxidation and assimilation were measured with (14)C-radiolabelled compounds in cultures of HTCC2181 and seawater microbial communities collected off the Oregon coast. The results indicated that in nature as well as in culture, C1 substrates are partitioned between those that are mainly oxidized to produce energy and those that are assimilated. These findings indicate that the combined fluxes of C1 compounds in coastal systems are sufficient to support significant populations of obligate methyltrophs by a metabolic strategy that involves the synergistic metabolism of multiple C1 compounds.

Methanol oxidation by temperate soils and environmental determinants of associated methylotrophs

“…PQQ MDH also occurs in many other Gram-negative methylotrophs (Nunn et al, 1989;Schmidt et al, 2010;Chistoserdova, 2011). Utilization of micro molar concentrations is known from M. extorquens AM1, and the marine methylotrophic strain HTCC2181 (Betaproteobacteria) (Giovannoni et al, 2008;Halsey et al, 2012). Strain HTCC2118 assimilates 10 mmol l À 1 methanol, which is substantially above observed minimal concentrations (0.002 mmol g soilDW À 1…”

“…Moreover, it has been demonstrated that methylotrophs that are restricted to methanol as carbon source exhibit increased methanol assimilation rates when they codissimilate alternative monocarbon compounds (Halsey et al, 2012). Thus, it is likely that methanol utilizers in aerated soils are not restricted to ambient methanol utilization and occupy different ecological niches in regard to the alternative substrates they can metabolize (Kolb, 2009a).…”

Insights into Denitrification in Methylotenera mobilis from Denitrification Pathway and Methanol Metabolism Mutants

“…The phenotypes of the xoxF mutants strongly suggest their involvement in methanol metabolism, identifying them as likely methanol dehydrogenases, with redundant functions. Such a role has been previously proposed for XoxF proteins (22,23), and weak methanol dehydrogenase activity has been measured for a purified XoxF protein from Methylobacterium extorquens AM1 (24). It is assumed that, like the MxaFI methanol dehydrogenase, the immediate electron acceptor is a cytochrome c (12).…”

Implications of streamlining theory for microbial ecology

“…OM43 is a coastal species that is found associated with phytoplankton (Morris et al, 2006). Recent reports of high turnover rates for methanol in the ocean surface (Dixon et al, 2011), a report describing many alternative OM43 substrates (trimethylamine, trimethylamine oxide, dimethylamine and methyl chloride; Halsey et al, 2012), and a report that OM43 xoxF was 2.3% of the identified spectra in a productive coastal ocean metaproteome (Sowell et al, 2011), all suggest future studies will aim to understand this unusual organism.…”