Methanotrophic symbionts provide carbon for photosynthesis in peat bogs

Abstract

Wetlands are the largest natural source of atmospheric methane 1 , the second most important greenhouse gas 2 . Methane flux to the atmosphere depends strongly on the climate 3 ; however, by far the largest part of the methane formed in wetland ecosystems is recycled and does not reach the atmosphere 4,5 . The biogeochemical controls on the efficient oxidation of methane are still poorly understood. Here we show that submerged Sphagnum mosses, the dominant plants in some of these habitats, consume methane through symbiosis with partly endophytic methanotrophic bacteria, leading to highly effective in situ methane recycling. Molecular probes revealed the presence of the bacteria in the hyaline cells of the plant and on stem leaves. Incubation with 13 C-methane showed rapid in situ oxidation by these bacteria to carbon dioxide, which was subsequently fixed by Sphagnum, as shown by incorporation of 13 C-methane into plant sterols. In this way, methane acts as a significant (10-15%) carbon source for Sphagnum. The symbiosis explains both the efficient recycling of methane and the high organic carbon burial in these wetland ecosystems.Peat bogs alternate between lawns and pools. Lawns are dominated by species that grow up to several decimetres above the water table. Pools are dominated by aquatic species, such as Sphagnum cuspidatum, that form layers of living plants below the water table. We investigated the methane-oxidizing activity of submerged S. cuspidatum from peat bog pools at different field locations in the Netherlands, and compared it to the activity of S. magellanicum and S. papillosum growing in lawns. The potential methane-oxidizing activity was substantially higher in the submerged mosses (Fig. 1). In control experiments with bog water, methane was not oxidized, indicating that the methanotrophic bacteria were mainly present on or in the living Sphagnum tissue.The identity and location of these methanotrophs was determined in a molecular approach. Total genomic DNA from washed Sphagnum plants was isolated and bacterial 16S ribosomal RNA genes were amplified, cloned into Escherichia coli, sequenced and analysed phylogenetically. One of the 16S rRNA gene sequences of the clone library was affiliated to a cluster of type II methanotrophs that contained acidophilic methanotrophs isolated from Sphagnum bogs, such as Methylocella palustris (identity 93%) 6 and Methylocapsa acidiphila (identity 93%) 7 .The full 16S rRNA gene sequence was used to design two specific oligonucleotide probes for fluorescence in situ hybridization (FISH). FISH was combined with serial sectioning of the stems and the stem leaves of multiple individuals of submerged S. cuspidatum. The methanotrophic bacterium targeted by the probes was the dominant methanotroph in S. cuspidatum sections, accounting for over 75% of

Development and refinement of proxy-climate indicators from peats

“…Higher methane fluxes under wet conditions lead to more assimilation of CH 4 -derived CO 2 and thus lower carbon isotopic ratios of Sphagnum biomarkers. Up to 15% of the CO 2 used by Sphagnum can come from recycled methane (Raghoebarsing et al, 2005). The amount of recycled CO 2 available to Sphagnum is influenced mainly by the wetness of the mire surface.…”

“…The first is the carbon isotope ratio of the CO 2 used for photosynthesis. A methanotrophic bacterium lives symbiotically with Sphagnum in its hyaline (water-holding) cells (Raghoebarsing et al, 2005).…”

A novel pathway of direct methane production and emission by eukaryotes including plants, animals and fungi: An overview

“…Methanotrophs have been previously identified only in CH 4 -rich environments, such as soil, fresh water and marine environments ). The products of CH 4 oxidation by methanotrophic symbionts in plants provide carbon for photosynthesis (Raghoebarsing et al, 2005). Numerous plants are suggested to harbour epiphytic methanotrophic bacteria.…”

Methanotrophy induces nitrogen fixation during peatland development

“…Because the growth and decomposition rates of Sphagnum mosses are greatly responsible for the C biosequestration in peatlands, the ecology of Sphagnum mosses is of particular interest. Recent studies have shown that Sphagnum mosses have an association with methanotrophic bacteria that leads to a reduction in methane (CH 4 ) emissions to the atmosphere and the provision of additional carbon dioxide (CO 2 ) source for the host plants (3,4). However, the growth of Sphagnum mosses in peatlands is often N limited, at least under low atmospheric N deposition (5), so biological fixation of atmospheric N 2 , i.e., the biological conversion of dinitrogen to plant-available ammonium, may stimulate moss growth (6).…”