Methanotrophs dominate methanogens and act as a methane sink in a subterranean karst cave

Xiaoyu Cheng; Zhilin Zeng; Xiaoyan Liu; Lu Li; Hongmei Wang; Rui Zhao; Paul L E Bodelier; Weiqi Wang; Yiheng Wang; Olli H Tuovinen

doi:10.1016/j.scitotenv.2023.164562

Methanotrophs dominate methanogens and act as a methane sink in a subterranean karst cave

Sci Total Environ. 2023 Sep 20:892:164562. doi: 10.1016/j.scitotenv.2023.164562. Epub 2023 May 29.

Authors

Xiaoyu Cheng¹, Zhilin Zeng², Xiaoyan Liu², Lu Li², Hongmei Wang³, Rui Zhao⁴, Paul L E Bodelier⁵, Weiqi Wang², Yiheng Wang², Olli H Tuovinen⁶

Affiliations

¹ State Key Laboratory of Biogeology and Environmental Geology, China University of Geosciences, Wuhan 430074, China; School of Environmental Studies, China University of Geosciences, Wuhan 430074, China; Department of Microbial Ecology, Netherlands Institute of Ecology (NIOO-KNAW), Droevendaalsesteeg 10, 6708 PB Wageningen, the Netherlands.
² State Key Laboratory of Biogeology and Environmental Geology, China University of Geosciences, Wuhan 430074, China; School of Environmental Studies, China University of Geosciences, Wuhan 430074, China.
³ State Key Laboratory of Biogeology and Environmental Geology, China University of Geosciences, Wuhan 430074, China; School of Environmental Studies, China University of Geosciences, Wuhan 430074, China. Electronic address: hmwang@cug.edu.cn.
⁴ Department of Earth, Atmospheric and Planetary Sciences, Massachusetts Institute of Technology, Cambridge, MA 02139, USA.
⁵ Department of Microbial Ecology, Netherlands Institute of Ecology (NIOO-KNAW), Droevendaalsesteeg 10, 6708 PB Wageningen, the Netherlands.
⁶ Department of Microbiology, Ohio State University, Columbus, OH 43210, USA.

PMID: 37257612
DOI: 10.1016/j.scitotenv.2023.164562

Abstract

Karst caves are potential sinks of atmospheric methane due to microbial consumption. However, knowledge gaps on methanogens (methane producing microorganisms) and their interaction with methane-oxidizing bacteria (MOB) hinder our further understanding about methane dynamics in karst caves. Here we reported methanogenic community composition and their interaction with MOBs in the Heshang Cave to comprehensively understand methane cycling in subsurface biosphere. MOBs in karst cave were dominated by high-affinity MOB, upland soil cluster (USC), with USCγ pmoA gene abundance within the range of 1.34 × 10⁴ to 1.8 × 10⁷ copies·g^-1 DW. In contrast, methanogens were dominated by Methanoregula and cluster ZC-I. The mcrA numbers were 7.21 × 10³ to 8.31 × 10⁴ copies·g^-1 DW, 1-3 orders of magnitude lower than those of MOB. The inter-domain network analysis indicated that MOBs and methanogens cooperated more in the interior of the cave. Despite of the higher number of methanogenic nodes in the network, MOB dominated the keystone taxa, suggesting a leading functional role of MOB. MOB in caves showed a comparable with or higher potential methane oxidizing rate (PMOR, 0.63 ng CH₄·g^-1 DW·h^-1 in sediment versus 11.02 ng CH₄·g^-1 DW·h^-1 in weathered rock) than those in soils, whereas methane produced by methanogens was undetected. Collectively, high absolute abundances of MOB, high PMORs, the dominance of methanotrophic keystone taxa in the inter-domain network confirmed the superiority of MOBs over methanogens in the oligotrophic karst cave, mounting new evidence on caves as an important methane sink in terms of the interaction between methanogens and MOBs.

Keywords: Inter-domain ecological network; Karst cave; Methane cycle; Methane sink; Methane-oxidizing bacteria; Methanogens.

MeSH terms

Caves / microbiology
Methane*
Methylococcaceae*
Soil
Soil Microbiology

Substances

Methane
Soil