Unexpected role of canonical aerobic methanotrophs in upland agricultural soils

authored by: Adrian Ho, Hyo Jung Lee, Max Reumer, Marion Meima-Franke, Ciska Raaijmakers, Hans Zweers, Wietse de Boer, Wim H. Van der Putten, Paul L.E. Bodelier
Abstract: Aerobic oxidation of methane at (circum-)atmospheric concentrations (<40 ppm_v) has long been assumed to be catalyzed by the as-yet-uncultured high-affinity methanotrophs in well-aerated, non-wetland (upland) soils, the only known biological methane sink globally. Although the low-affinity canonical methanotrophs with cultured representatives have been detected along with the high-affinity ones, their role as a methane sink in upland soils remains enigmatic. Here, we show that canonical methanotrophs can contribute to (circum-)atmospheric methane uptake in agricultural soils. We performed a stable-isotope ¹³C–CH₄ labelling incubation in the presence and absence of bio-based residues that were added to the soil to track the flow of methane. Residue amendment transiently stimulated methane uptake rate (<50 days). Soil methane uptake was sustained throughout the incubation (130 days), concomitant to the enrichment of ¹³C–CO₂. The ¹³C-enriched phospholipid fatty acids (PLFAs) were distinct in both soils, irrespective of amendments, and were unambiguously assigned almost exclusively to canonical alphaproteobacterial methanotrophs with cultured representatives. 16S rRNA and pmoA gene sequence analyses revealed that the as-yet-uncultured high-affinity methanotrophs were virtually absent in these soils. The stable-isotope labelling approach allowed to attribute soil methane uptake to canonical methanotrophs, whereas these were not expected to consume (circum-)atmospheric methane. Our findings thus revealed an overlooked reservoir of high-affinity methane-oxidizers represented by the canonical methanotrophs in agriculture-impacted upland soils. Given that upland agricultural soils have been thought to marginally or do not contribute to atmospheric methane consumption due to the vulnerability of the high-affinity methanotrophs, our findings suggest a thorough revisiting of the contribution of agricultural soils, and the role of agricultural management to mitigation of climate change.
Organisation(s): Institute of Microbiology
External Organisation(s): Netherlands Institute of Ecology
Kunsan National University
Wageningen University and Research
Type: Article
Journal: Soil Biology and Biochemistry
Volume: 131
Pages: 1-8
No. of pages: 8
ISSN: 0038-0717
Publication date: 04.2019
Publication status: Published
Peer reviewed: Yes
ASJC Scopus subject areas: Microbiology, Soil Science
Sustainable Development Goals: SDG 2 - Zero Hunger, SDG 13 - Climate Action, SDG 15 - Life on Land
Electronic version(s): https://pure.knaw.nl/portal/en/publications/unexpected-role-of-canonical-aerobic-methanotrophs-in-upland-agri (Access: Open)
https://doi.org/10.1016/j.soilbio.2018.12.020 (Access: Closed)