Unexpected role of canonical aerobic methanotrophs in upland agricultural soils

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

*Corresponding author for this work

Research output: Contribution to journalArticleAcademicpeer-review

4 Citations (Scopus)

Abstract

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.

Original languageEnglish
Pages (from-to)1-8
Number of pages8
JournalSoil Biology and Biochemistry
Volume131
DOIs
Publication statusPublished - 1 Apr 2019

Fingerprint

methanotrophs
upland soils
Methane
agricultural soils
agricultural soil
methane
Soil
soil
Isotope Labeling
isotope labeling
stable isotopes
stable isotope
incubation
agricultural management
Climate Change
soil amendments
phospholipid
Agriculture
rRNA Genes
oxidants

Keywords

  • C labelling
  • High-affinity methane oxidation
  • Methylocystaceae
  • PLFA analysis/ land-use change
  • pmoA

Cite this

Ho, A., Lee, H. J., Reumer, M., Meima-Franke, M., Raaijmakers, C., Zweers, H., ... Bodelier, P. L. E. (2019). Unexpected role of canonical aerobic methanotrophs in upland agricultural soils. Soil Biology and Biochemistry, 131, 1-8. https://doi.org/10.1016/j.soilbio.2018.12.020
Ho, Adrian ; Lee, Hyo Jung ; Reumer, Max ; Meima-Franke, Marion ; Raaijmakers, Ciska ; Zweers, Hans ; de Boer, Wietse ; Van der Putten, Wim H. ; Bodelier, Paul L.E. / Unexpected role of canonical aerobic methanotrophs in upland agricultural soils. In: Soil Biology and Biochemistry. 2019 ; Vol. 131. pp. 1-8.
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Unexpected role of canonical aerobic methanotrophs in upland agricultural soils. / Ho, Adrian; Lee, Hyo Jung; Reumer, Max; Meima-Franke, Marion; Raaijmakers, Ciska; Zweers, Hans; de Boer, Wietse; Van der Putten, Wim H.; Bodelier, Paul L.E.

In: Soil Biology and Biochemistry, Vol. 131, 01.04.2019, p. 1-8.

Research output: Contribution to journalArticleAcademicpeer-review

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.

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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

U2 - 10.1016/j.soilbio.2018.12.020

DO - 10.1016/j.soilbio.2018.12.020

M3 - Article

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JF - Soil Biology and Biochemistry

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