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. 2024 Aug 16:15:1423245.
doi: 10.3389/fmicb.2024.1423245. eCollection 2024.

Genomic and physiological properties of Anoxybacterium hadale gen. nov. sp. nov. reveal the important role of dissolved organic sulfur in microbial metabolism in hadal ecosystems

Junwei Cao #  1 , Baoying Shao #  1 , Jing Lin  1 , Jie Liu  1 , Yiran Cui  1 , Jiahua Wang  1 , Jiasong Fang  1   2
Affiliations

Genomic and physiological properties of Anoxybacterium hadale gen. nov. sp. nov. reveal the important role of dissolved organic sulfur in microbial metabolism in hadal ecosystems

Junwei Cao et al. Front Microbiol. .

Abstract

Hadal zones account for the deepest 45% of the oceanic depth range and play an important role in ocean biogeochemical cycles. As the least-explored aquatic habitat on earth, hadal ecosystems contain a vast diversity of so far uncultured microorganisms that cannot be grown on conventional laboratory culture media. Therefore, it has been difficult to gain a true understanding of the detailed metabolic characteristics and ecological functions of those difficult-to-culture microorganisms in hadal environments. In this study, a novel anaerobic bacterial strain, MT110T, was isolated from a hadal sediment-water interface sample of the Mariana Trench at 10,890 m. The level of 16S rRNA gene sequence similarity and percentage of conserved proteins between strain MT110T and the closest relatives, Anaerovorax odorimutans DSM 5092T (94.9 and 46.6%) and Aminipila butyrica DSM 103574T (94.4 and 46.7%), indicated that strain MT110T exhibits sufficient molecular differences for genus-level delineation. Phylogenetic analyses based on both 16S rRNA gene and genome sequences showed that strain MT110T formed an independent monophyletic branch within the family Anaerovoracaceae. The combined evidence showed that strain MT110T represents a novel species of a novel genus, proposed as Anoxybacterium hadale gen. nov. sp. nov. (type strain MT110T = KCTC 15922T = MCCC 1K04061T), which represents a previously uncultured lineage of the class Clostridia. Physiologically, no tested organic matter could be used as sole carbon source by strain MT110T. Genomic analysis showed that MT110T had the potential capacity of utilizing various carbon sources, but the pathways of sulfur reduction were largely incomplete. Our experiments further revealed that cysteine is one of the essential nutrients for the survival of strain MT110T, and cannot be replaced by sulfite, leucine, or taurine. This result suggests that organic sulfur compounds might play an important role in metabolism and growth of the family Anaerovoracaceae and could be one of the key factors affecting the cultivation of the uncultured microbes. Our study brings a new perspective to the role of dissolved organic sulfur in hadal ecosystems and also provides valuable information for optimizing the conditions of isolating related microbial taxa from the hadal environment.

Keywords: Clostridia bacterium; cysteine; hadal environment; organic sulfur; uncultured microbe.

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Conflict of interest statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Figures

Figure 1
Figure 1
Maximum-likelihood tree showing the phylogenetic positions of strain MT110T and related species, based on 16S rRNA gene sequences. Bootstrap values ≥50% (expressed as percentages of 1,000 replications) are shown at branch nodes. Bar, 0.05 nucleotide substitution rate (Knuc) units. Defluviitalea saccharophila LIND6LT2T (HQ020487) was used as outgroup.
Figure 2
Figure 2
Phylogeny of strain MT110T and the related species based on 120 concentration proteins. Strain MT110T and a closely related metagenome-assembled genome (UBA7709) are highlighted in red and blue, respectively. The black nodes mean the bootstrap values ≥70%.
Figure 3
Figure 3
Schematic overview of the metabolic potential of strain MT110T. The red arrows indicate no path exists.
Figure 4
Figure 4
Effect of different substrates on growth of strain MT110T in BMY medium. (A) and (B), results of two independent experiments; 1 and 7, BYM control; 2, glucose; 3, xylose; 4, fructose; 5, inositol; 6, ribose; 8, sucrose; 9, cellobiose; 10, starch. *p ≤ 0.05, **p ≤ 0.01, ***p ≤ 0.001, ****p ≤ 0.0001.
Figure 5
Figure 5
Effect of cysteine and methionine on growth of strain MT110T in BM medium with 0.025% (A) and 0.05% (B) reducing agent (Na2S·9H2O). 1, 18 amino acids (except cysteine and methionine); 2, 18 amino acids and methionine; 3, 18 amino acids and cysteine; 4, 18 amino acids and methionine, cysteine. nsp > 0.05, no significant correlation; *p ≤ 0.05, **p ≤ 0.01, ***p ≤ 0.001.
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References

    1. Aromokeye D. A., Oni O. E., Tebben J., Yin X., Friedrich M. W. (2020). Crystalline iron oxides stimulate methanogenic benzoate degradation in marine sediment-derived enrichment cultures. ISME J. 15, 965–980. doi: 10.1038/s41396-020-00824-7 - DOI - PMC - PubMed
    1. Balch W. E., Fox G. E., Magrum L. J., Woese C. R., Wolfe R. S. (1979). Methanogens: reevaluation of a unique biological group. Microbiol. Rev. 43, 260–296. doi: 10.1128/mr.43.2.260-296.1979, PMID: - DOI - PMC - PubMed
    1. Bertelli C., Laird M. R., Williams K. P., Simon Fraser University Research Computing, G. Lau B. Y., Hoad G., et al. . (2017). IslandViewer 4: expanded prediction of genomic islands for larger-scale datasets. Nucleic Acids Res. 45, W30–W35. doi: 10.1093/nar/gkx343 - DOI - PMC - PubMed
    1. Brock T. D., Od'ea K. (1977). Amorphous ferrous sulfide as a reducing agent for culture of anaerobes. Appl. Environ. Microbiol. 33, 254–256. doi: 10.1128/aem.33.2.254-256.1977, PMID: - DOI - PMC - PubMed
    1. Cao J., Gayet N., Zeng X., Shao Z., Jebbar M., Alain K. (2016). Pseudodesulfovibrio indicus gen. nov., sp. nov., a piezophilic sulfate-reducing bacterium from the Indian Ocean and reclassification of four species of the genus Desulfovibrio. Int. J. Syst. Evol. Microbiol. 66, 3904–3911. doi: 10.1099/ijsem.0.001286, PMID: - DOI - PubMed

Grants and funding

The author(s) declare that financial support was received for the research, authorship, and/or publication of this article. This study was funded by the National Natural Science Foundation of China (Grant Nos. 91951210 and 92251303) and the Marine Biomedical Science and Technology Innovation Platform of Lin-gang Special Area.

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