TY - JOUR

T1 - Unexpected role of canonical aerobic methanotrophs in upland agricultural soils

AU - Ho, Adrian

AU - Lee, Hyo Jung

AU - Reumer, Max

AU - Meima-Franke, Marion

AU - Raaijmakers, Ciska

AU - Zweers, Hans

AU - de Boer, Wietse

AU - Van der Putten, Wim H.

AU - Bodelier, Paul L.E.

N1 - Funding information: We are grateful to Iris Chardon for excellent technical assistance. We extend our gratitude to Mattias de Hollander for assistance during the sequence analysis. AH is financially supported by the BE-Basic grant F03.001 (SURE/SUPPORT), and from funds by the Deutsche Forschungsgemeinschaft (DFG grant HO 6234/1-1 ) and the Leibniz Universität Hannover (Germany) . This publication is publication no. 6657 of the Netherlands Institute of Ecology.

PY - 2019/4

Y1 - 2019/4

N2 - Aerobic oxidation of methane at (circum-)atmospheric concentrations (<40 ppmv) 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.

AB - Aerobic oxidation of methane at (circum-)atmospheric concentrations (<40 ppmv) 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.

KW - C labelling

KW - High-affinity methane oxidation

KW - Methylocystaceae

KW - PLFA analysis/ land-use change

KW - pmoA

UR - http://www.scopus.com/inward/record.url?scp=85059194626&partnerID=8YFLogxK

U2 - 10.1016/j.soilbio.2018.12.020

DO - 10.1016/j.soilbio.2018.12.020

M3 - Article

AN - SCOPUS:85059194626

VL - 131

SP - 1

EP - 8

JO - Soil Biology and Biochemistry

JF - Soil Biology and Biochemistry

SN - 0038-0717

ER -