Abstract
Sediments underlying marine hypoxic zones are huge sinks of unreacted complex organic matter, where despite acute O2 limitation, obligately aerobic bacteria thrive, and steady depletion of organic carbon takes place within a few meters below the seafloor. However, little knowledge exists about the sustenance and complex carbon degradation potentials of aerobic chemoorganotrophs in these sulfidic ecosystems. We isolated and characterized a number of aerobic bacterial chemoorganoheterotrophs from across a ~ 3 m sediment horizon underlying the perennial hypoxic zone of the eastern Arabian Sea. High levels of sequence correspondence between the isolates’ genomes and the habitat’s metagenomes and metatranscriptomes illustrated that the strains were widespread and active across the sediment cores explored. The isolates catabolized several complex organic compounds of marine and terrestrial origins in the presence of high or low, but not zero, O2. Some of them could also grow anaerobically on yeast extract or acetate by reducing nitrate and/or nitrite. Fermentation did not support growth, but enabled all the strains to maintain a fraction of their cell populations over prolonged anoxia. Under extreme oligotrophy, limited growth followed by protracted stationary phase was observed for all the isolates at low cell density, amid high or low, but not zero, O2 concentration. While population control and maintenance could be particularly useful for the strains’ survival in the critically carbon-depleted layers below the explored sediment depths (core-bottom organic carbon: 0.5–1.0% w/w), metagenomic data suggested that in situ anoxia could be surmounted via potential supplies of cryptic O2 from previously reported sources such as Nitrosopumilus species.
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Data availability
GenBank accession numbers for the 16S rRNA genes, genomes, and plasmids (if any) of the new isolates are as follows: Brevibacterium sp. BDJS002/MCC 5171-OQ780597, CP116392; Brevibacterium sp. JSBI002/MCC 5172-OQ780604, CP110341; Brucella sp. JSBI001/MCC 5134-OQ780596, CP110339, CP110340; Gordonia hongkongensis SMJS1/MCC 5348-OQ780429, CP123381, CP123382, CP123383; Halomonas sp. BDJS001/MCC 5128-OQ780651, CP110535; Halopseudomonas bauzanensis SMJS2/MCC 5363-OQ780586, CP123445, CP123446; Marinobacter segnicrescens AN1/MCC 5129-OQ780700, CP110342; Mesobacillus sp. SBJS01-OQ780701, CP109811; Stenotrophomonas sp. SBJS02/MCC 5130-OQ780703, CP109812.
All nucleotide sequence data have been deposited in NCBI Sequence Read Archive (SRA) or GenBank under the BioProject accession number PRJNA309469:
The complete circular genome or plasmid sequences of the pure culture strains isolated have the GenBank accession numbers CP109811, CP109812, CP110339 through CP110342, CP110535, CP116392, CP123381 through CP123383, CP123445, and CP123446.
The whole metagenome shotgun sequence datasets have the Run Accession numbers SRR3646127, SRR3646128, SRR3646129, SRR3646130, SRR3646131, SRR3646132, SRR3646144, SRR3646145, SRR3646147, SRR3646148, SRR3646150, SRR3646151, SRR3646152, SRR3646153, SRR3646155, SRR3646156, SRR3646157, SRR3646158, SRR3646160, SRR3646161, SRR3646162, SRR3646163, SRR3646164, SRR3646165; SRR3570036, SRR3570038, SRR3577067, SRR3577068, SRR3577070, SRR3577071, SRR3577073, SRR3577076, SRR3577078, SRR3577079, SRR3577081, SRR3577082, SRR3577086, SRR3577087, SRR3577090, SRR3577311, SRR3577337, SRR3577338, SRR3577341, SRR3577343, SRR3577344, SRR3577345, SRR3577347, SRR3577349, SRR3577350, and SRR3577351.
The whole metatranscriptome shotgun sequence datasets have the Run Accession numbers SRR7967962, SRR9596399, SRR7983762, SRR9597791, and SRR7992674.
The sequence datasets obtained via PCR amplification of the V4-V5 regions of Nitrosopumilus-specific 16S rRNA genes have the Run Accession numbers SRR24121604, SRR24121705, SRR24121602, SRR24121623, SRR24123082, SRR24122693, SRR24121664, SRR24121706, SRR24121641, SRR24121637, SRR24121644, SRR24121647, SRR24121642, SRR24122688, SRR24122690, SRR24121638, SRR24121640, SRR24121648, SRR24121663, SRR24121649, SRR24121645, SRR24123085, SRR24122686, SRR24121636, and SRR24121643.
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Acknowledgements
We express gratitude to the Director of CSIR-National Institute of Oceanography for enabling the research cruise SSK42. Support extended by the CSIR-NIO Ship Cell and crew members of SSK42 is recognized gratefully. J.S. and S.D. received fellowships from Council of Scientific and Industrial Research, Government of India (GoI). M.M. and S.C. received fellowships from the Department of Biotechnology, GoI. S.B., N.M. and S.N. got their fellowships from Bose Institute.
Funding
The microbiological studies were funded by Bose Institute (via Intramural Faculty Grants) and Earth System Science Organization, Ministry of Earth Sciences (MoES), GoI via the extramural grant MoES/36/00IS/Extra/19/2013; the research cruise SSK42 was also funded by MoES (GAP2303).
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W.G. conceived the study, designed the experiments, interpreted the results, and wrote the paper. J.S. planned and performed the experiments, analyzed and curated the data, and also composed the paper. A.M. led the SSK42 mission and all geochemical studies therein; A.M. and A.P. made intellectual contributions to the present paper. M.M. performed microbiological experiments, while S.B., S.D., S.C., N.M., and S.N. performed omics studies. All authors read and ratified the manuscript.
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Sarkar, J., Mondal, M., Bhattacharya, S. et al. Extremely oligotrophic and complex-carbon-degrading microaerobic bacteria from Arabian Sea oxygen minimum zone sediments. Arch Microbiol 206, 179 (2024). https://doi.org/10.1007/s00203-024-03875-y
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DOI: https://doi.org/10.1007/s00203-024-03875-y