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A dominant subgroup of marine Bathyarchaeia assimilates organic and inorganic carbon into unconventional membrane lipids

Nature Microbiology volume 10, pages 2579–2590 (2025)Cite this article

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Abstract

Bathyarchaeia, an abundant and ecologically versatile archaea found commonly in marine sediments, has a key role in the global carbon cycle. However, its lipid biomarkers and carbon assimilation mechanisms are poorly understood. Here, using a highly enriched Bathyarchaeia culture (>95% archaea) obtained from estuarine sediment of the East China Sea, we show that Baizosediminiarchaeum (formerly subgroup Bathy-8), the most abundant and widespread Bathyarchaeia group on Earth, synthesizes butanetriol dialkyl glycerol tetraethers (BDGTs) as its dominant membrane lipids. BDGTs are unusual archaeal tetraether lipids characterized by a butanetriol backbone instead of the typical glycerol, challenging fundamental assumptions in archaeal lipid biochemistry. Although BDGTs have been previously identified in the methanogen Methanomassiliicoccus luminyensis, we now provide direct evidence that Bathyarchaeia also synthesizes BDGTs, definitively establishing this globally abundant group as a natural BDGT producer. Stable isotope probing with 13C-bicarbonate shows that Baizosediminiarchaeum assimilates carbon into BDGTs from both inorganic carbon and lignin. These unique carbon assimilation strategies suggest the biogeochemical importance of Baizosediminarchaeum in marine carbon cycling and organic matter decomposition.

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Fig. 1: Global distribution patterns of Bathyarchaeia subgroups in marine sediments.
Fig. 2: BDGT-0 structure and LC–MS detection of Bathyarchaeia-derived lipids.
Fig. 3: Archaeal community dynamics and lipid profiles across cultivation time points.
Fig. 4: Isotopic fractionation of BDGT-derived biphytane from 13C-labelled DIC and unlabelled lignin.

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Data availability

The 16S rRNA gene sequencing data from the East China Sea (Fig. 1) have been deposited in the NCBI SRA under accession number PRJNA1303662 and in the National Omics Data Encyclopedia under accession number OEP00006462. Mass spectrometry data supporting Fig. 2 and Extended Data Fig. 2 are publicly available via Zenodo at https://doi.org/10.5281/zenodo.16742269 (ref. 63). Stable isotope data supporting Fig. 4 are available via Zenodo at https://doi.org/10.5281/zenodo.16748030 (ref. 64). Source data are provided with this paper.

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Acknowledgements

We thank W. Wu for his insightful suggestions on stable isotope probing techniques, as well as L. Deng, S. Ding, H. Zhang and H. Hu for their valuable comments during the revision process. We also thank W. Zhang and Q. Luo at the State Key Laboratory of Microbial Metabolism, School of Life Science and Biotechnology, Shanghai Jiao Tong University, for their generous support with mass spectrometry analyses. This work was supported financially by the Natural Science Foundation of China (grants 42230401 to F.W. and 42472370 to L.D.), the Postdoctoral Fellowship Program (Grade B) of China Postdoctoral Science Foundation (GZB20240430 to J.H.), 2030 Project of Shanghai Jiao Tong University (grant WH510244001), Global Subseafloor Ecosystem and Sustainability (GSES) and the project ‘Ocean Negative Carbon Emission (ONCE)’.

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Author notes

  1. Xiaoxiao Zhao

    Present address: Leibniz Laboratory for Radiometric Dating and Stable Isotope Research, Kiel University, Kiel, Germany

  2. These authors contributed equally: Liang Dong, Yunge Jing.

Authors and Affiliations

  1. State Key Laboratory of Submarine Geoscience; Key Laboratory of Polar Ecosystem and Climate Change, Ministry of Education; Shanghai Key Laboratory of Polar Life and Environment Sciences; and School of Oceanography, Shanghai Jiao Tong University, Shanghai, China

    Liang Dong, Jialin Hou, Jiaming Zhou, Tiantian Yu, Shijie Chen, Lewen Liang, Pengfei Zhu & Fengping Wang

  2. State Key Laboratory of Microbial Metabolism, School of Life Science and Biotechnology, Shanghai Jiao Tong University, Shanghai, China

    Yunge Jing, Xiaoxiao Zhao & Fengping Wang

  3. MARUM—Center for Marine Environmental Sciences and Faculty of Geosciences, University of Bremen, Bremen, Germany

    Kai-Uwe Hinrichs

  4. Southern Marine Science and Engineering Guangdong Laboratory (Zhuhai), Zhuhai, China

    Fengping Wang

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Contributions

L.D. and F.W. designed the study, and K.-U.H. supervised the study thoroughly. L.D., Y.J., J.H., J.Z., T.Y., S.C., L.L., P.Z. and X.Z. performed the research. L.D., Y.J., J.H., J.Z., S.C., X.Z. and K.-U.H. analysed the data. L.D., Y.J., K.-U.H. and F.W. wrote the paper.

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Correspondence to Fengping Wang.

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Extended data

Extended Data Fig. 1 Quantitative analysis of cellular lipid content in cultured samples.

Quantification of cellular core lipids content in isoprenoid glycerol dibiphytanyl glycerol tetraethers (IPL-derived CLs) following acid hydrolysis over a harvest time of 120 days. The dashed lines indicate the lower and upper bounds (0.7 and 1.5 fg/cell, respectively) for the estimated cellular lipid content derived from a cellular geometry model. Bathyarchaeia biomass was additionally quantified using quantitative PCR (qPCR).

Source data

Extended Data Fig. 2 Extracted mass chromatogram of core lipids.

The core lipids were derived from normal-phase UPLC-APCI-QTOF analysis of extract obtained from acid hydrolysis of Bathyarchaeia cells.

Source data

Extended Data Fig. 3 Archaeal community structure and core lipid composition following cell acid hydrolysis.

a, Abundance of Bathyarchaeia, estimated by 16S rRNA gene copy numbers after 30 days’ incubation. Data are presented as mean values ± SD (n = 3 biological replicates; independent culture bottles). b, Archaeal community composition at the phylum/class level (left) and Bathyarchaeia subgroup/genus level (right). The Bathyarchaeia community was primarily composed of Baizosediminiarchaeum (93.4%), with Baizomonas comprising 6.5%. “Others” refers to unclassified archaeal taxa. c, Composition of core lipids (CLs) released after acid hydrolysis of archaeal cells. The left bar shows the total distribution of major lipid classes—archaeol (AR), butanetriol dialkyl glycerol tetraethers (BDGTs), and glycerol dialkyl glycerol tetraethers (GDGTs). The right bar displays the relative proportions of individual BDGT (BDGT-0 to BDGT-2) and GDGT (GDGT-0 to GDGT-3) homologues.

Source data

Extended Data Fig. 4 Proposed carbon isotope fractionation and metabolic pathways in Bathyarchaeia.

This schematic highlight key carbon isotope fractionation processes and metabolic pathways involved in lipids synthesis by Bathyarchaeia. δ¹³C values and fractionation factors (ε) for different carbon pools and metabolites are shown. The primary carbon sources, dissolved inorganic carbon (DIC) and lignin, are utilization at an approximate ratio of 1:2. Fractionation factors between BP0 and DIC (εBP0/DIC), and BP0 and lignin (εBP0/Lignin) are -36.1‰ and -52.1‰, respectively. The pathways illustrated include demethylation (conversion of lignin to -CH₃-THMPT), acetyl-CoA formation (from acetate), the Wood-Ljungdahl (WL) pathway (conversion of CO₂ to acetyl-CoA via carbon monoxide dehydrogenase/acetyl-CoA synthase (CODH/ACS))11, and the role of carbonic anhydrase (CA) in HCO₃⁻ to CO₂ conversion65. This schematic emphasizes the contributions of DIC and lignin to lipid biosynthesis and highlights the isotope fractionation associated with these metabolic pathways.

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Dong, L., Jing, Y., Hou, J. et al. A dominant subgroup of marine Bathyarchaeia assimilates organic and inorganic carbon into unconventional membrane lipids. Nat Microbiol 10, 2579–2590 (2025). https://doi.org/10.1038/s41564-025-02121-5

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