Atmospheric methane consumption in arid ecosystems acts as a reverse chimney and is accelerated by plant-methanotroph biomes

Delherbe, Nathalie A.; Gomez, Oscar; Plominsky, Alvaro M.; Oliver, Aaron; Manzanera, Maximino; Kalyuzhnaya, Marina G.

doi:10.1093/ismejo/wraf026

Title: Atmospheric methane consumption in arid ecosystems acts as a reverse chimney and is accelerated by plant-methanotroph biomes

Journal Article · 01 March 2025 · The ISME Journal

DOI: https://doi.org/10.1093/ismejo/wraf026 · OSTI ID:2543112

Delherbe, Nathalie A. ^[1]; Gomez, Oscar ^[1]; Plominsky, Alvaro M. ^[2]; Oliver, Aaron ^[2]; Manzanera, Maximino ^[3]; Kalyuzhnaya, Marina G. ^[1]

San Diego State Univ., CA (United States)
Univ. of California, San Diego, CA (United States). Scripps Inst. of Oceanography
Univ. of Granada (Spain)

Drylands cover one-third of the Earth’s surface and are one of the largest terrestrial sinks for methane. Understanding the structure–function interplay between members of arid biomes can provide critical insights into mechanisms of resilience toward anthropogenic and climate-change-driven environmental stressors—water scarcity, heatwaves, and increased atmospheric greenhouse gases. This study integrates in situ measurements with culture-independent and enrichment-based investigations of methane-consuming microbiomes inhabiting soil in the Anza-Borrego Desert, a model arid ecosystem in Southern California, United States. The atmospheric methane consumption ranged between 2.26 and 12.73 μmol m² h⁻¹, peaking during the daytime at vegetated sites. Metagenomic studies revealed similar soil-microbiome compositions at vegetated and unvegetated sites, with Methylocaldum being the major methanotrophic clade. Eighty-four metagenome-assembled genomes were recovered, six represented by methanotrophic bacteria (three Methylocaldum, two Methylobacter, and uncultivated Methylococcaceae). The prevalence of copper-containing methane monooxygenases in metagenomic datasets suggests a diverse potential for methane oxidation in canonical methanotrophs and uncultivated Gammaproteobacteria. Five pure cultures of methanotrophic bacteria were obtained, including four Methylocaldum. Genomic analysis of Methylocaldum isolates and metagenome-assembled genomes revealed the presence of multiple stand-alone methane monooxygenase subunit C paralogs, which may have functions beyond methane oxidation. Furthermore, these methanotrophs have genetic signatures typically linked to symbiotic interactions with plants, including tryptophan synthesis and indole-3-acetic acid production. Based on in situ fluxes and soil microbiome compositions, we propose the existence of arid-soil reverse chimneys, an empowered methane sink represented by yet-to-be-defined cooperation between desert vegetation and methane-consuming microbiomes.

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Research Organization:: San Diego State Univ., CA (United States); Univ. of California, San Diego, CA (United States). Scripps Inst. of Oceanography; Univ. of Granada (Spain)

Sponsoring Organization:: USDOE; USDOE Joint Genome Institute (JGI); USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: SC0024289

OSTI ID:: 2543112

Report Number(s):: RPT-0000026099

Journal Information:: The ISME Journal, Journal Name: The ISME Journal Journal Issue: 1 Vol. 19; ISSN 1751-7362; ISSN 1751-7370

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

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59 BASIC BIOLOGICAL SCIENCES
Methylocaldum
arid soil
desert microbiomes
methane cycle
methanotrophs
plants

Title: Atmospheric methane consumption in arid ecosystems acts as a reverse chimney and is accelerated by plant-methanotroph biomes

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