Bark-dwelling methanotrophic bacteria decrease methane emissions from trees

Jeffrey, Luke C.; Maher, Damien T.; Chiri, Eleonora; Leung, Pok Man; Nauer, Philipp A.; Arndt, Stefan K.; Tait, Douglas R.; Greening, Chris; Johnston, Scott G

doi:10.21203/rs.3.rs-119818/v1

Cited by 3 publications

(10 citation statements)

References 50 publications

(69 reference statements)

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“…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.…”

Section: Discussionmentioning

confidence: 99%

“…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.…”

Section: Discussionmentioning

confidence: 99%

“…(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):

α = [\frac{normall normalo g_{e} ()(, \frac{δ^{13} C_{t} + 1000}{δ^{13} C_{t = 0} + 1000})}{normall normalo g_{e} ()(, \frac{M}{M_{0}})}]

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.…”

Section: Methodsmentioning

confidence: 99%

“…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.…”

Section: Introductionmentioning

confidence: 99%

“…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.…”

Section: Introductionmentioning

confidence: 99%

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

et al. 2021

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Summary Knowledge regarding mechanisms moderating methane (CH4) sink/source behaviour along the soil–tree stem–atmosphere continuum remains incomplete. Here, we applied stable isotope analysis (δ13C‐CH4) to gain insights into axial CH4 transport and oxidation in two globally distributed subtropical lowland species (Melaleuca quinquenervia and Casuarina glauca). We found consistent trends in CH4 flux (decreasing with height) and δ13C‐CH4 enrichment (increasing with height) in relation to stem height from ground. The average lower tree stem δ13C‐CH4 (0–40 cm) of Melaleuca and Casuarina (−53.96‰ and −65.89‰) were similar to adjacent flooded soil CH4 ebullition (−52.87‰ and −62.98‰), suggesting that stem CH4 is derived mainly by soil sources. Upper stems (81–200 cm) displayed distinct δ13C‐CH4 enrichment (Melaleuca −44.6‰ and Casuarina −46.5‰, respectively). Coupled 3D‐photogrammetry with novel 3D‐stem measurements revealed distinct hotspots of CH4 flux and isotopic fractionation on Melaleuca, which were likely due to bark anomalies in which preferential pathways of gas efflux were enhanced. Diel experiments revealed greater δ13C‐CH4 enrichment and higher oxidation rates in the afternoon, compared with the morning. Overall, we estimated that c. 33% of the methane was oxidised between lower and upper stems during axial transport, therefore potentially representing a globally significant, yet previously unaccounted for, methane sink.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

α = [\frac{normall normalo g_{e} ()(, \frac{δ^{13} C_{t} + 1000}{δ^{13} C_{t = 0} + 1000})}{normall normalo g_{e} ()(, \frac{M}{M_{0}})}]

Section: Methodsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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

et al. 2021

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Riparian Cottonwood Trees and Adjacent River Sediments Have Different Microbial Communities and Produce Methane With Contrasting Carbon Isotope Compositions

et al. 2022

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Rivers and their adjacent riparian forests are intimately linked by the exchange of water, nutrients, and organic matter. Both riparian cottonwood trees and adjacent river sediments host microbial communities including archeal methanogens, supporting methane production and emission to the atmosphere. Here we combine microbial community and in vitro stable isotope analyses to characterize the drivers of methane cycling in distinct anoxic habitats (river sediments vs. riparian cottonwood stems) associated with the Oldman River, southern Alberta (Canada). We demonstrate that, differences in the chemical characteristics of organic matter support divergent microbial communities that generate methane from distinct metabolic pathways. Organic matter in river sediments had C/N ratios approximately 50‐fold lower than in tree stems and had more diverse dissolved organic components. Contrasting substrate availability between river sediment and tree stems was likely the primary mechanism for the greater microbial diversity in river sediments than in tree stems, the significantly different bacterial communities, and the trend toward differing abundance of methanogen orders. The methane carbon isotope composition (δ13C values) differed for the tree stem (−103.6‰ to −70.6‰) and river sediment (−55.1‰ to −48.4‰) environments, suggesting that methane was primarily produced via CO2‐reduction in tree stems by Methanobacteriales, while river sediments produced more methane through acetate fermentation primarily by Methanosarcinales. This study demonstrates the importance of organic matter quality and microbial community composition in driving metabolic processes contributing to methane production and emission in rivers and adjacent riparian forests.

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Spatiotemporal variability and origin of CO₂ and CH₄ tree stem fluxes in an upland forest

Barba

Poyatos

Capooci

et al. 2021

Global Change Biology

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The exchange of multiple greenhouse gases (i.e., CO2 and CH4) between tree stems and the atmosphere represents a knowledge gap in the global carbon cycle. Stem CO2 and CH4 fluxes vary across time and space and are unclear, which are their individual or shared drivers. Here we measured CO2 and CH4 fluxes at different stem heights combining manual (biweekly; n = 678) and automated (hourly; n > 38,000) measurements in a temperate upland forest. All trees showed CO2 and CH4 emissions despite 20% of measurements showing net CH4 uptake. Stem CO2 fluxes presented clear seasonal trends from manual and automated measurements. Only automated measurements captured the high temporal variability of stem CH4 fluxes revealing clear seasonal trends. Despite that temporal integration, the limited number of automated chambers made stand‐level mean CH4 fluxes sensitive to “hot spots,” resulting in mean fluxes with high uncertainty. Manual measurements provided better integration of spatial variability, but their lack of temporal variability integration hindered the detection of temporal trends and stand‐level mean fluxes. These results highlight the potential bias of previous studies of stem CH4 fluxes solely based on manual or automated measurements. Stem height, temperature, and soil moisture only explained 7% and 11% of the stem CH4 flux variability compared to 42% and 81% for CO2 (manual and automated measurements, respectively). This large unexplained variability, in combination with high CH4 concentrations in the trees' heartwood, suggests that stem CH4 fluxes might be more influenced by gas transport and diffusivity through the wood than by drivers of respiratory CO2 flux, which has crucial implications for developing process‐based ecosystem models. We postulate that CH4 is likely originated within tree stems because of lack of a consistent vertical pattern in CH4 fluxes, evidence of CH4 production in wood incubations, and low CH4 concentration in the soil profile but high concentrations within the trees' heartwood.

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Bark-dwelling methanotrophic bacteria decrease methane emissions from trees

Cited by 3 publications

References 50 publications

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

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

Riparian Cottonwood Trees and Adjacent River Sediments Have Different Microbial Communities and Produce Methane With Contrasting Carbon Isotope Compositions

Spatiotemporal variability and origin of CO₂ and CH₄ tree stem fluxes in an upland forest

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Bark-dwelling methanotrophic bacteria decrease methane emissions from trees

Cited by 3 publications

References 50 publications

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

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

Riparian Cottonwood Trees and Adjacent River Sediments Have Different Microbial Communities and Produce Methane With Contrasting Carbon Isotope Compositions

Spatiotemporal variability and origin of CO2 and CH4 tree stem fluxes in an upland forest

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Spatiotemporal variability and origin of CO₂ and CH₄ tree stem fluxes in an upland forest