Bark microbiota modulate climate-active gas fluxes in Australian forests.

Recent studies suggest that microbes inhabit tree bark, yet little is known about their identities, functions, and environmental roles. Here we reveal, through gene-centric and genome-resolved metagenomics, that the bark of eight common Australian tree species hosts abundant and specialized microbial communities. The predominant bacteria are hydrogen-cycling facultative anaerobes adapted to dynamic redox and substrate conditions. Furthermore, bark-associated methanotrophs are abundant and can coexist with hydrogenotrophic methanogens. Microcosm experiments showed that bark microorganisms aerobically consume methane, hydrogen, and carbon monoxide at in planta concentrations and produce these gases under anoxia. Combined with in situ field measurements, we show that tree-dwelling microbiota metabolize multiple climate-active gases at marked rates within tree stems, highlighting a potentially substantial role in global atmospheric cycles. Editor's summary: Tree trunks comprise a huge area of habitat for metabolically active microorganisms. Not only do the trunks provide a substrate for many epiphytic species, but tree bark also shelters specific communities of bacteria. Leung et al. sampled the bark of several eastern Australian trees to investigate the species present and their metabolic capacities. Depending on locality, prevailing conditions, and species and their microbiota, tree trunk communities can be net producers or consumers of climate active gases. While planning a planting scheme, it is therefore important to assess specific settings for the potential role that trees can play, through their trunk communities, in climate mitigation (see the Perspective by Gauci). —Caroline Ash INTRODUCTION: The global surface area of tree bark is similar to that of terrestrial Earth. These substantial tree surfaces are increasingly recognized for mediating the exchange of atmospheric gases along the soil-tree-atmosphere continuum. They also represent a potential habitat for microorganisms, with recent metabarcoding studies indicating a possible role for bark microbes in the cycling of methane (CH4). However, a general understanding of the metabolism and ecosystem roles of these potentially globally pervasive microbiota remains lacking. RATIONALE: At the soil-atmosphere interface, we predicted that tree bark microbiota use diverse gas substrates to sustain growth and in turn may mediate an important role in global atmospheric gas cycling. However, previous metabarcoding approaches have only provided limited and indirect inference for the lifestyle of bark microorganisms. Numerous traits, such as microbial oxidation of the climate-active gases hydrogen (H2) and carbon monoxide (CO), cannot be reliably predicted by taxonomic affiliation. A functional understanding of the bark microbiota requires direct evidence from genomic characterization and functional validation. Here we integrated genome-resolved metagenomic analysis with in situ and ex situ biogeochemical assays to study the capabilities, metabolism, and ecosystem importance of bark microbiota in Australian forests. RESULTS: We examined bark microbiota of eight prevalent Australian tree species, spanning freshwater wetland, coastal, and upland forest biomes. All tree species were found to harbor abundant endophytic microbial populations, estimated at up to 6 trillion cells per square meter of bark. Gene-centric and genome-resolved metagenomics revealed that bark microbial communities were distinct from surrounding soils and waters and included diverse metabolically flexible gas cycling and facultatively anaerobic bacteria. Predominant bacteria were predicted to consume hydrogen through aerobic respiration and fermentatively produce this gas during hypoxia. Bacteria encoding enzymes for aerobic and anaerobic metabolism of other gases, including CO, CH4, and volatile organic compounds, were also abundant, with methanogenic archaea present in some wetland trees. Consistently, microcosm assays showed that bark microorganisms aerobically consume CH4, H2, and CO but switched to production of these gases under anoxia. In situ measurements further showed that fluxes of multiple climate-active gases occur at tree bark surfaces. In particular, net H2 uptake was consistently observed across all tree species and bark heights, indicating that bark may be an overlooked H2 sink, where robust microbial activity could account for annual removal of atmospheric H2 at the teragram scale. CONCLUSION: Our results provided genome-resolved insights into the abundant bark microbiota, revealing their ability to flexibly metabolize gases and adapt to substrate and redox conditions within trees. Their activities substantially modulate fluxes of major climate-active gases, such as CH4, and the often-overlooked indirect greenhouse gases H2, CO, and volatile organic compounds. Bark microbiota may contribute to the climate benefits of trees by removing multiple climate-active gases, although their metabolic flexibility indicates a potential to switch to a source, depending upon environmental conditions. Collectively, these results suggest that trees and their microbiota contribute to regulating global atmospheric cycles and should be considered in biogeochemical models, forest management, and conservation efforts. Tree bark are microbiological and biogeochemical hotspots for climate-active gas cycling.: Trees act as conduits linking soils and the atmosphere, facilitating gas exchange and as a niche for microbial communities adapted to metabolizing gas substrates. Together, trees and bark microbiota function as a modulator of the emission and uptake of multiple climate-active gases in forest ecosystems. [ABSTRACT FROM AUTHOR]