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A Marine Group A isolate relies on other growing bacteria for cell wall formation

Nature Microbiology volume 9, pages 1954–1963 (2024)Cite this article

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Abstract

Most of Earth’s prokaryotes live under energy limitation, yet the full breadth of strategies that enable survival under such conditions remain poorly understood. Here we report the isolation of a bacterial strain, IA91, belonging to the candidate phylum Marine Group A (SAR406 or ‘Candidatus Marinimicrobia’) that is unable to synthesize the central cell wall compound peptidoglycan itself. Using cultivation experiments and microscopy, we show that IA91 growth and cell shape depend on other bacteria, deriving peptidoglycan, energy and carbon from exogenous muropeptide cell wall fragments released from growing bacteria. Reliance on exogenous muropeptides is traceable to the phylum’s ancestor, with evidence of vertical inheritance across several classes. This dependency may be widespread across bacteria (16 phyla) based on the absence of key peptidoglycan synthesis genes. These results suggest that uptake of exogenous cell wall components could be a relevant and potentially common survival strategy in energy-limited habitats like the deep biosphere.

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Fig. 1: Changes in IA91 cell morphology with culture conditions.
Fig. 2: Muropeptide metabolisms in IA91.
Fig. 3: Comparative genomics analyses.

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Data availability

Sequence data that support the findings of this study have been deposited in NCBI Sequence Read Archive under Bioproject accession numbers PRJDB13945 (IA91 genome) and PRJDB17482 (RNA-seq). Other genome sequences used in this study are available in GTDB. All unique biological materials (that is, strains Acc8 and IA91) are available at Japan Collection of Microorganisms (JCM) in RIKEN-BRC under accession numbers JCM 39386 (Acc8) and JCM 39387 (IA91). Raw microscopic images are available via Zenodo at https://doi.org/10.5281/zenodo.10617219 (ref. 62). Source data are provided with this paper.

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Acknowledgements

We acknowledge the Kanto Natural Gas Development Co., Ltd. for collecting samples at their facilities. We also thank C. Miyako, R. Iwanami and M. Ogawara for assistance in molecular analyses and F. Nozawa and S. Yamaoka for assistance in cultivation experiments. The ampG-deficient cells of E. coli K-12 BW25113 were provided by the National Bio-Resource Project (NIG, Japan): E. coli. This work was supported by JSPS KAKENHI grant numbers 17K15183 (T.K.), 18H03367 (M.K.N.), 18H02426 (H.T.), 18H05295 (Y.K.), 22H04985 (H.I.) and 23K18158 (T.K.).

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Author notes

  1. These authors contributed equally: Taiki Katayama, Masaru K. Nobu.

Authors and Affiliations

  1. Research Institute for Geo-Resources and Environment, Geological Survey of Japan (GSJ), National Institute of Advanced Industrial Science and Technology (AIST), Tsukuba, Japan

    Taiki Katayama & Hideyoshi Yoshioka

  2. Bioproduction Research Institute, AIST, Tsukuba, Japan

    Masaru K. Nobu, Xian-Ying Meng, Kana Morinaga, Yoichi Kamagata & Hideyuki Tamaki

  3. Institute for Extra-Cutting-Edge Science and Technology Avant-Garde Research (X-star), Japan Agency for Marine–Earth Science and Technology (JAMSTEC), Yokosuka, Japan

    Masaru K. Nobu & Hiroyuki Imachi

  4. EM Application Department, EM Business Unit, JEOL, Ltd., Akishima, Japan

    Naoki Hosogi

  5. Research Institute of Earthquake and Volcano Geology, GSJ, AIST, Tsukuba, Japan

    Hiroshi A. Takahashi

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Contributions

T.K., M.K.N. and H.T. designed the study. T.K., M.K.N., Y.K. and H.T. wrote the paper. T.K., H.Y. and H.I. performed the cultures, and T.K. isolated strains Acc8 and IA91. T.K. and M.K.N. performed bioinformatic analyses. T.K. and K.M. performed phase-contrast and fluorescence microscopy. X.-Y.M. performed scanning and transmission electron microscopy. N.H. performed cryo-electron microscopy. H.A.T. and H.Y. performed stable carbon isotopic analysis. All authors reviewed the results and approved the paper.

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Correspondence to Taiki Katayama.

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Extended data

Extended Data Fig. 1 Phylogenetic tree of IA91 and MG-A members.

Phylogenomic tree (maximum-likelihood tree) of strain IA91 (bold red), clone MK-334 (bold) and relatives in Marine Group A based on a concatenated alignment of ribosomal proteins. Metagenome-assembled genomes of representatives in Genome Taxonomy Database with CheckM completeness ≥ 85% and contamination ≤ 5% were selected for the analysis. The previously-used clade names are indicated in parentheses. Asterisks in nodes denote low bootstrap values, that is, ultrafast bootstrap approximation < 95% or SH-like approximate likelihood ratio test (SH-aLRT) support < 80%.

Extended Data Fig. 2 Effect of ampicillin treatment on IA91 cell morphology.

Representative phase-contrast micrographs before treatment (after one week of cultivation) (a), after 24h treatment (b) and without treatment (c). SYBR Green I was used to stain DNA (right panels). n=3 independent experiments. (Scale bars: 5 µm).

Extended Data Fig. 3 Peptidoglycan staining of ampicillin-treated IA91 cells.

Peptidoglycan (PG) staining of IA91 cells showing the presence of PG layer in rod-shaped cells but not in coccoids. Ampicillin-treated cells from pure culture were stained with Alexa Flour 488 dye-labeled wheat germ agglutinin (WGA) and visualized using phase-contrast (left), fluorescent microscopy (middle) and overlay images (right). Cells were treated with ampicillin for shorter time frame (12 h) compared with those in Extended Data Fig. 2 so as to observe both rod- and sphere-shaped cells in the same condition. Coccoids with local staining are indicated by blue arrows, whereas non-stained coccoids are indicated by black arrows. n=3 independent experiments. (Scale bars: 5 µm).

Extended Data Fig. 4 The occurrence of IA91 growth in cultures supplemented with peptidoglycan-derived compounds.4.

The final concentration of each compound in the culture medium was 10 µg ml−1. IA91 growth was determined by CH4 production after one month of cultivation and microscopy after 10 days of cultivation. IA91 was cultured with H2-utilizing Methanothermobacter thermautotrophicus strain ΔH. For CH4 production, means ± standard deviation of triplicate cultures are shown (a). CH4 detection limit was 0.5 mM. Representative phase-contrast micrographs are shown (b-i). SYBR Green I was used to stain DNA (b-i). Cells of co-cultured M. thermautotrophicus strain ∆H are visible in cyan due to their F420 autofluorescence. n=3 independent experiments. Abbreviation; PG, peptidoglycan; MP, muropeptide; MurNAc, N-acetylmuramic acid; GlcNAc, N-acetylglucosamine; AA, PG amino acids (that is, D-Ala, D-Glu and L-Lys). (Scale bars: 5 µm, b-i).

Extended Data Fig. 5 The presence of PG synthesis and recycle proteins within the members of the classes UBA2242, AB16 and UBA8477.

Corresponding to each lineage, the presence/absence of specific proteins are indicated by the heatmap. Asterisk indicates the clade to which strain IA91 and clone MK-334 belongs.

Source data

Extended Data Fig. 6 Phylogenetic tree of MurB within MG-A.

Comparison of phylogenetic tree of MurB (left) and concatenated ribosomal proteins (right) within Marine Group A showing horizontal transfer of MurB gene to the classes SORT01, JAANXI01, UBA2242 and Ca. Marinisomatia. Nodes having low statistical support values (ultrabootstrap approximation < 95%) were removed from the tree.

Extended Data Fig. 7 Phylogenetic tree of MurA within MG-A.

Comparison of phylogenetic tree of MurA (left) and concatenated ribosomal proteins (right) within Marine Group A. Nodes having low statistical support values (ultrabootstrap approximation < 95%) were removed from the tree.

Extended Data Fig. 8 Phylogenetic tree of cytochrome c oxidase subunit 1 within MG-A.

Comparison of phylogenetic tree of cytochrome c oxidase subunit 1 (left) and concatenated ribosomal proteins (right) within Marine Group A showing horizontal transfer of cytochrome c oxidase subunit 1 gene to the classes SORT01, JAANXI01, UBA8477 and Ca. Marinisomatia. Nodes having low statistical support values (ultrabootstrap approximation < 95%) were removed from the tree.

Supplementary information

Supplementary Information

Supplementary Figs. 1–13 and Tables 1–4.

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Supplementary Table 5

Phylogenetic distribution of genomes that lack MurA and MurB genes.

Supplementary Data 2

Statistical source data for Supplementary Figs. 5, 7 and 11.

Source data

Source Data Fig. 1

Statistical source data for Fig. 1.

Source Data Fig. 3

Statistical source data for Fig. 3.

Source Data Extended Data Fig. 5

Statistical source data for Extended Data Fig. 5.

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Katayama, T., Nobu, M.K., Imachi, H. et al. A Marine Group A isolate relies on other growing bacteria for cell wall formation. Nat Microbiol 9, 1954–1963 (2024). https://doi.org/10.1038/s41564-024-01717-7

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