Bark-dwelling methanotrophic bacteria decrease methane emissions from trees

Abstract

Tree stems are an important and unconstrained source of methane, yet it is uncertain if there are internal microbial controls (i.e. methanotrophy) within tree bark, that may reduce methane emissions. Using multiple lines of evidence, we demonstrate here that unique microbial communities dominated by methane oxidising bacteria (MOB) dwell within bark of Melaleuca quinquenervia, a common, invasive and globally distributed lowland species. Laboratory incubations of methane inoculated M. quinquenervia bark reveal methane consumption (up to 96.3 µmol m-2 bark d-1) and distinct isotopic δ13C-CH4 enrichment characteristic of MOB. Molecular analysis indicates unique microbial communities reside within the bark, with methane-oxidising bacteria primarily from the genus Methylomonas comprising up to 25 % of the total microbial community. Methanotroph abundance was linearly correlated to methane uptake rates (R2 = 0.76, p = 0.006). Finally, field-based methane oxidation inhibition experiments demonstrate that bark-dwelling MOB reduce methane emissions by 36 ± 5 %. These multiple, complementary lines of evidence indicate that bark-dwelling MOB represent a novel and potentially significant methane sink, and an important frontier for further research.

Isotopic evidence for axial tree stem methane oxidation within subtropical lowland forests

“…However, methanogens were shown to be in relatively low abundance in the bark‐dwelling microbial community of Melaleuca stems from the same Melaleuca forest (Av. 0.8%; range 0.2–2.5%) (Jeffrey et al ., 2021). The Melaleuca bark communities were dominated by hydrogenotrophic methanogens members of the genus Methanobacterium , known for their relatively high tolerance of oxygen (Kiener & Leisinger, 1983), and differed from the metabolically versatile methanogens of the genus Methanosarcina dominating the methanogenic community of sediments in close proximity (Jeffrey et al ., 2021; sequence data publicly available under NCBI BioProject accession no.…”

“…Mass‐dependent fractionation may potentially contribute to observed trends, in which atomically lighter CH 4 molecules ( 12 C‐CH 4 ) preferentially travel and de‐gas faster upwards and outwards compared with the slightly heavier isotope ( 13 C‐CH 4 ). However, MOB (primarily from the genus Methylomonas ) have been shown to be abundant in lowland Melaleuca bark, comprising up to 25% of the total microbial community (Jeffrey et al ., 2021). The MOB relative abundance in bark far exceeded the MOB relative abundance in the adjacent wetland soils and aquatic microbial communities (average 0.2% and 6.1% in relative abundance, respectively, from 16S rRNA gene amplicon sequencing analysis), suggesting that bark‐dwelling MOB are both uniquely adapted to and highly abundant within the stems of some high CH 4 fluxing lowland forests.…”

“…(2020b). Using the MOB fractionation factor (α) measured from previous laboratory‐based CH 4 inoculation of Melaleuca quinquenervia bark samples (1.031 ± 0.014, n = 16) (Jeffrey et al ., 2021), we calculated the CH 4 oxidised ( M o ) between the lower stem and upper stem by first solving for M o according to Coleman et al . (1981):where M is the total amount of methane, t is time, t = 0 are initial conditions, and then compared the ratio of M – M o (measured) vs M – M o (solved for oxidation; O x ), with the difference between these two assumed to be the diffusive flux.…”

“…Additionally, the phenomenon of axial decreases in CH 4 flux may also be partially explained by a recently discovered biological CH 4 sink with bark‐associated methanotrophic bacteria shown to mediate significant rates of CH 4 via oxidation within tree stems both in situ and under controlled laboratory conditions (Jeffrey et al , 2021). However, it remains to be understood how this CH 4 sink varies between sampling location, tree species and tree tissues.…”

“…Whilst various communities of methanotrophs and methylotrophs can inhabit the phyllosphere (Doronina et al ., 2004; Iguchi et al ., 2012, 2015; Knief et al ., 2012), in woody tree tissues, methane‐oxidising bacteria (MOB) abundance compared with the total microbial community ranges from < 1% in the heartwood of upland Populus deltoides (Yip et al ., 2019) up to c . 25% in tree stems of lowland Melaleuca quinquenervia (Jeffrey et al ., 2021). However, their functionality and ability to moderate tree stem methane emissions remains more broadly unknown.…”