Riverbed methanotrophy sustained by high carbon conversion efficiency

Abstract

Our understanding of the role of freshwaters in the global carbon cycle is being revised, but there is still a lack of data, especially for the cycling of methane, in rivers and streams. Unravelling the role of methanotrophy is key to determining the fate of methane in rivers. Here we focus on the carbon conversion efficiency (CCE) of methanotrophy, that is, how much organic carbon is produced per mole of CH4 oxidised, and how this is influenced by variation in methanotroph communities. First, we show that the CCE of riverbed methanotrophs is consistently high (~50%) across a wide range of methane concentrations (~10–7000 nM) and despite a 10-fold span in the rate of methane oxidation. Then, we show that this high conversion efficiency is largely conserved (50%± confidence interval 44–56%) across pronounced variation in the key functional gene (70 operational taxonomic units (OTUs)), particulate methane monooxygenase (pmoA), and marked shifts in the abundance of Type I and Type II methanotrophs in eight replicate chalk streams. These data may suggest a degree of functional redundancy within the variable methanotroph community inhabiting these streams and that some of the variation in pmoA may reflect a suite of enzymes of different methane affinities which enables such a large range of methane concentrations to be oxidised. The latter, coupled to their high CCE, enables the methanotrophs to sustain net production throughout the year, regardless of the marked temporal and spatial changes that occur in methane.

Spatial separation of anaerobic ammonium oxidation and nitrite‐dependent anaerobic methane oxidation in permeable riverbeds

“…Candidatus Methylomirabilis oxyfera, which oxidizes methane using internally produced oxygen (Ettwig et al, 2010;Wu et al, 2011), is known to be sensitive to external free oxygen (Luesken et al, 2012); though trace oxygen (0.7%-1.1% of O 2 ) has actually been reported to stimulate n-damo activity in enrichment cultures, albeit only moderately (Kampman et al, 2018). Further, in the more permeable gravels, it is also likely that the growth and activity of n-damo bacteria are limited by strong competition for methane from aerobic methanotrophs, whose activity has been recorded in a wide range of gravel riverbeds (Shelley et al, 2014;Trimmer et al, 2015). Even though the bulk pore water of sandy riverbeds still has appreciable oxygen (> 38 μM), ndamo can occur in such riverbeds, probably due to the presence of anoxic microsites within aggregates as observed for anammox (Lansdown et al, 2016).…”

Physiological Ecology of Microorganisms in Subglacial Lake Whillans

“…The oxygen demand for methane oxidation was determined using estimated rates of methane oxidation (Michaud, 2016). We used the stoichiometry for methane oxidation shown in Table S2, and assumed that the fraction of methane incorporated into biomass was 0.5 (a median value across habitats; Shelley et al, 2014; Trimmer et al, 2015), resulting in 1.5 mol O 2 consumed per mol of CH 4 oxidized.…”

Bringing methanotrophy in rivers out of the shadows

“…The capacity for methane oxidation was calculated using linear regression of nmol CH 4 consumed per hour during the linear phase of the incubation (72 h) and then normalized for dry mass of sediment. Using this measured capacity for methane oxidation (C mo , nmol CH 4 g 21 dry sediment h 21 ) a site-specific rate (i.e., predicted rate in situ, taking account of ambient concentration at that site) was calculated using well estimated linear relationships (typically R 2 5 0.96, error on slope 4%) which holds well beyond the range of adjustment applied here (Shelley et al 2014Trimmer et al 2015):…”

“…(2) Whereby, R mo is the rate of methane oxidation (nmol g 21 h 21 ), V is the volume in cm 3 taken up by 1 g of gravel (0.95), CCE is the carbon conversion efficiency which we have shown previously to be 0.5 (50%) for eight typical chalk streams (see Trimmer et al 2015), d is the depth over which we have integrated the methane oxidation [15 cm is the conservative estimate of riverbed depth over which methane oxidation occurs at a similar rate to that at the surface (Shelley et al 2014)]; and h is the number of hours (per day) over which methanotrophy was assumed to occur (24). For the artificial channels experiment, d was set at 5 cm as this was the depth of gravel in the channels.…”