Lipidomic diversity and proxy implications of archaea from cold seep sediments of the South China Sea

Tingting Zhang; Wei He; Qianyong Liang; Fengfeng Zheng; Xi Xiao; Zhiyu Zeng; Jingzhuo Zhou; Wenyong Yao; Haodong Chen; Yuanqing Zhu; Jing Zhao; Yan Zheng; Chuanlun Zhang

doi:10.3389/fmicb.2023.1241958

Lipidomic diversity and proxy implications of archaea from cold seep sediments of the South China Sea

Front Microbiol. 2023 Oct 19:14:1241958. doi: 10.3389/fmicb.2023.1241958. eCollection 2023.

Authors

Tingting Zhang^#^{1

2

3}, Wei He^#⁴, Qianyong Liang^{1

2

5}, Fengfeng Zheng⁴, Xi Xiao^{1

2}, Zhiyu Zeng⁴, Jingzhuo Zhou⁶, Wenyong Yao⁴, Haodong Chen⁷, Yuanqing Zhu^{4

8}, Jing Zhao¹, Yan Zheng^{4

9}, Chuanlun Zhang^{4

5

8}

Affiliations

¹ Guangzhou Marine Geological Survey, China Geological Survey, Guangzhou, China.
² National Engineering Research Center of Gas Hydrate Exploration and Development, Guangzhou, China.
³ East China Sea Ecological Center, Ministry of Natural Resources, Shanghai, China.
⁴ Shenzhen Key Laboratory of Marine Archaea Geo-Omics, Department of Ocean Science and Engineering, Southern University of Science and Technology, Shenzhen, China.
⁵ Southern Marine Science and Engineering Guangdong Laboratory (Guangzhou), Guangzhou, China.
⁶ Key Laboratory of Coal Processing and Efficient Utilization of Ministry of Education, School of Chemical Engineering and Technology, China University of Mining and Technology, Xuzhou, China.
⁷ State Key Laboratory of Organic Geochemistry, Guangzhou Institute of Geochemistry, Chinese Academy of Sciences, Guangzhou, China.
⁸ Shanghai Sheshan National Geophysical Observatory, Shanghai, China.
⁹ School of Environmental Science and Engineering, Southern University of Science and Technology, Shenzhen, China.

^# Contributed equally.

Abstract

Cold seeps on the continental margins are characterized by intense microbial activities that consume a large portion of methane by anaerobic methanotrophic archaea (ANME) through anaerobic oxidation of methane (AOM). Although ANMEs are known to contain unique ether lipids that may have an important function in marine carbon cycling, their full lipidomic profiles and functional distribution in particular cold-seep settings are still poorly characterized. Here, we combined the 16S rRNA gene sequencing and lipidomic approaches to analyze archaeal communities and their lipids in cold seep sediments with distinct methane supplies from the South China Sea. The archaeal community was dominated by ANME-1 in the moderate seepage area with strong methane emission. Low seepage area presented higher archaeal diversity covering Lokiarchaeia, Bathyarchaeia, and Thermoplasmata. A total of 55 core lipids (CLs) and intact polar lipids (IPLs) of archaea were identified, which included glycerol dialkyl glycerol tetraethers (GDGTs), hydroxy-GDGTs (OH-GDGTs), archaeol (AR), hydroxyarchaeol (OH-AR), and dihydroxyarchaeol (2OH-AR). Diverse polar headgroups constituted the archaeal IPLs. High concentrations of dissolved inorganic carbon (DIC) with depleted δ¹³C_DIC and high methane index (MI) values based on both CLs (MI_CL) and IPLs (MI_IPL) indicate that ANMEs were active in the moderate seepage area. The ANME-2 and ANME-3 clades were characterized by enhanced glycosidic and phosphoric diether lipids production, indicating their potential role in coupling carbon and phosphurus cycling in cold seep ecosystems. ANME-1, though representing a smaller proportion of total archaea than ANME-2 and ANME-3 in the low seepage area, showed a positive correlation with MI_IPL, indicating a different mechanism contributing to the IPL-GDGT pool. This also suggests that MI_IPL could be a sensitive index to trace AOM activities performed by ANME-1. Overall, our study expands the understanding of the archaeal lipid composition in the cold seep and improves the application of MI using intact polar lipids that potentially link to extent ANME activities.

Keywords: ANMEs; South China Sea; archaeal lipid biomarkers; cold seeps; methane index.