Volume 43 Issue 8
Aug.  2024
Turn off MathJax
Article Contents
Fei Xu, Xiang Zeng, Yadong Gong, Zongze Shao. Thiosulfate oxidation and autotrophy potential by marine prevalent heterotrophic bacteria of genus Marinobacter[J]. Acta Oceanologica Sinica, 2024, 43(8): 89-97. doi: 10.1007/s13131-023-2263-x
Citation: Fei Xu, Xiang Zeng, Yadong Gong, Zongze Shao. Thiosulfate oxidation and autotrophy potential by marine prevalent heterotrophic bacteria of genus Marinobacter[J]. Acta Oceanologica Sinica, 2024, 43(8): 89-97. doi: 10.1007/s13131-023-2263-x

Thiosulfate oxidation and autotrophy potential by marine prevalent heterotrophic bacteria of genus Marinobacter

doi: 10.1007/s13131-023-2263-x
Funds:  The National Natural Science Foundation of China under contract Nos 91951201 and 42030412; the National Key R&D Program of China under contract No. 2021YFF0501304; the Scientific Research Foundation of Third Institute of Oceanography, MNR under contract No. 2019021.
More Information
  • The genus Marinobacter is very broadly distributed in global environments and is considered as aerobic heterotroph. In this study, six Marinobacter strains were identified with autotrophic thiosulfate oxidation capacity. These strains, namely Marinobacter guineae M3BT, Marinobacter aromaticivorans D15-8PT, Marinobacter vulgaris F01T, Marinobacter profundi PWS21T, Marinobacter denitrificans JB02H27T, and Marinobacter sp. ST-1M (with a 99.93% similarity to the 16S rDNA sequences of Marinobacter salsuginis SD-14BT), were screened out of 32 Marinobacter strains by autotrophic thiosulfate oxidization medium. The population of cells grew in a chemolithotrophic medium, increasing from 105 cells/mL to 107 cells/mL within 5 d. This growth was accompanied by the consumption of thiosulfate 3.59 mmol/L to 9.64 mmol/L and the accumulation of sulfate up to 0.96 mmol/L, and occasionally produced sulfur containing complex particles. Among these Marinobacter strains, it was also found their capability of oxidizing thiosulfate to sulfate in a heterotrophic medium. Notably, M. vulgaris F01T and M. antarcticus ZS2-30T showed highly significant production of sulfate at 9.45 mmol/L and 3.10 mmol/L. Genome annotation indicated that these Marinobacter strains possess a complete Sox cluster for thiosulfate oxidation. Further phylogenetic analysis of the soxB gene revealed that six Marinobacter strains formed a separate lineage within Gammaproteobacteria and close to obligate chemolithoautotroph Thiomicrorhabdus arctica. The results indicated that thiosulfate oxidizing and chemolithoautotrophic potential in Marinobacter genus, which may contribute to the widespread of Marinobacter in the global ocean.
  • loading
  • Aziz R K, Bartels D, Best A A, et al. 2008. The RAST Server: rapid annotations using subsystems technology. BMC Genomics, 9: 75, doi: 10.1186/1471-2164-9-75
    Behera B C, Patra M, Dutta S K, et al. 2014. Isolation and characterisation of sulphur oxidising bacteria from mangrove soil of Mahanadi River Delta and their sulphur oxidising ability. Journal of Applied & Environmental Microbiology, 2(1): 1–5, doi: 10.12691/jaem-2-1-1
    Boroujeni S R, Kalbasi M, Asgharzadeh A, et al. 2021. Evaluating the potential of Halothiobacillus bacteria for sulfur oxidation and biomass production under saline soil. Geomicrobiology Journal, 38(1): 57–65, doi: 10.1080/01490451.2020.1809571
    Camacho C, Coulouris G, Avagyan V, et al. 2009. BLAST+: architecture and applications. BMC Bioinformatics, 10: 421, doi: 10.1186/1471-2105-10-421
    Chaudhary S, Tanvi, Dhanker R, et al. 2019. Different applications of sulphur oxidizing bacteria: a review. International Journal of Current Microbiology and Applied Sciences (IJCMAS), 8(11): 770–778, doi: 10.20546/ijcmas.2019.811.091
    Chen Zhiwei, Koh M, Van Driessche G, et al. 1994. The structure of flavocytochrome c sulfide dehydrogenase from a purple phototrophic bacterium. Science, 266(5184): 430–432, doi: 10.1126/science.7939681
    Choi B R, Pham V H, Park S J, et al. 2009. Characterization of facultative sulfur-oxidizing Marinobacter sp. BR13 isolated from marine sediment of Yellow Sea, Korea. Journal of the Korean Society for Applied Biological Chemistry, 52(4): 309–314, doi: 10.3839/jksabc.2009.055
    Cooper Z S, Rapp J Z, Shoemaker A M D, et al. 2022. Evolutionary divergence of Marinobacter strains in cryopeg brines as revealed by pangenomics. Frontiers in Microbiology, 13: 879116, doi: 10.3389/fmicb.2022.879116
    Dahl C. 2015. Cytoplasmic sulfur trafficking in sulfur-oxidizing prokaryotes. IUBMB Life, 67(4): 268–274, doi: 10.1002/iub.1371
    Dahl C. 2017. Sulfur metabolism in phototrophic bacteria. In: Hallenbeck P C, ed. Modern Topics in the Phototrophic Prokaryotes: Metabolism, Bioenergetics, and Omics. Cham: Springer, 27–66
    Denkmann K, Grein F, Zigann R, et al. 2012. Thiosulfate dehydrogenase: a widespread unusual acidophilic c-type cytochrome. Environmental Microbiology, 14(10): 2673–2688, doi: 10.1111/j.1462-2920.2012.02820.x
    Ding Wei, Wang Shougang, Qin Peng, et al. 2023. Anaerobic thiosulfate oxidation by the Roseobacter group is prevalent in marine biofilms. Nature Communications, 14(1): 2033, doi: 10.1038/s41467-023-37759-4
    Dou Le, Zhang Mengyu, Pan Luqing, et al. 2022. Sulfide removal characteristics, pathways and potential application of a novel chemolithotrophic sulfide-oxidizing strain, Marinobacter sp. SDSWS8. Environmental Research, 212: 113176, doi: 10.1016/j.envres.2022.113176
    Du Rui, Gao Di, Wang Yiting, et al. 2022. Heterotrophic sulfur oxidation of Halomonas titanicae SOB56 and its habitat adaptation to the hydrothermal environment. Frontiers in Microbiology, 13: 888833, doi: 10.3389/fmicb.2022.888833
    Edgar R C. 2004. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research, 32(5): 1792–1797, doi: 10.1093/nar/gkh340
    Felsenstein J. 1981. Evolutionary trees from DNA sequences: a maximum likelihood approach. Journal of Molecular Evolution, 17(6): 368–376, doi: 10.1007/BF01734359
    Fritz G, Roth A, Schiffer A, et al. 2002. Structure of adenylylsulfate reductase from the hyperthermophilic Archaeoglobus fulgidus at 1.6-Å resolution. Proceedings of the National Academy of Sciences of the United States of America, 99(4): 1836–1841, doi: 10.1073/pnas.042664399
    Gauthier M J, Lafay B, Christen R, et al. 1992. Marinobacter hydrocarbonoclasticus gen. nov. , sp. nov. , a new, extremely halotolerant, hydrocarbon-degrading marine bacterium. International Journal of Systematic and Evolutionary Microbiology, 42(4): 568–576, doi: 10.1099/00207713-42-4-568
    Ghosh W, Dam B. 2009. Biochemistry and molecular biology of lithotrophic sulfur oxidation by taxonomically and ecologically diverse bacteria and archaea. FEMS Microbiology Reviews, 33(6): 999–1043, doi: 10.1111/j.1574-6976.2009.00187.x
    Griesbeck C, Schütz M, Schödl T, et al. 2002. Mechanism of sulfide-quinone reductase investigated using site-directed mutagenesis and sulfur analysis. Biochemistry, 41(39): 11552–11565, doi: 10.1021/bi026032b
    Handley K M, Hery M, Lloyd J R. 2009. Marinobacter santoriniensis sp. nov. , an arsenate-respiring and arsenite-oxidizing bacterium isolated from hydrothermal sediment. International Journal of Systematic and Evolutionary Microbiology, 59(Pt 4): 886–892, doi: 10.1099/ijs.0.003145-0
    Handley K M, Lloyd J R. 2013. Biogeochemical implications of the ubiquitous colonization of marine habitats and redox gradients by Marinobacter species. Frontiers in Microbiology, 4: 136, doi: 10.3389/fmicb.2013.00136
    He Yang, Zeng Xiang, Xu Fei, et al. 2023. Diversity of mixotrophic neutrophilic thiosulfate- and iron-oxidizing bacteria from deep-sea hydrothermal vents. Microorganisms, 11(1): 100, doi: 10.3390/microorganisms11010100
    Hensen D, Sperling D, Trüper H G, et al. 2006. Thiosulphate oxidation in the phototrophic sulphur bacterium Allochromatium vinosum. Molecular Microbiology, 62(3): 794–810, doi: 10.1111/j.1365-2958.2006.05408.x
    Houghton J L, Foustoukos D I, Flynn T M, et al. 2016. Thiosulfate oxidation by Thiomicrospira thermophila: metabolic flexibility in response to ambient geochemistry. Environmental Microbiology, 18(9): 3057–3072, doi: 10.1111/1462-2920.13232
    Kumar S, Stecher G, Li Michael, et al. 2018. MEGA X: molecular evolutionary genetics analysis across computing platforms. Molecular Biology and Evolution, 35(6): 1547–1549, doi: 10.1093/molbev/msy096
    Lian Fengbai, Chen Xuyang, Jiang Shan, et al. 2021. Marinobacter orientalis sp. nov. , a thiosulfate-oxidizing bacterium isolated from a marine solar saltern. Antonie van Leeuwenhoek, 114(6): 765–775,doi: 10.1007/s10482-021-01556-0
    Montes M J, Bozal N, Mercadé E. 2008. Marinobacter guineae sp. nov. , a novel moderately halophilic bacterium from an Antarctic environment. International Journal of Systematic and Evolutionary Microbiology, 58(Pt 6): 1346–1349, doi: 10.1099/ijs.0.65298-0
    Na S I, Kim Y O, Yoon S H, et al. 2018. UBCG: up-to-date bacterial core gene set and pipeline for phylogenomic tree reconstruction. Journal of Microbiology, 56(4): 280–285, doi: 10.1007/s12275-018-8014-6
    Pott A S, Dahl C. 1998. Sirohaem sulfite reductase and other proteins encoded by genes at the dsr locus of Chromatium vinosum are involved in the oxidation of intracellular sulfur. Microbiology, 144(Pt 7): 1881–1894, doi: 10.1099/00221287-144-7-1881
    Rana K, Rana N, Singh B. 2020. Applications of sulfur oxidizing bacteria. In: Salwan R, Sharma V, eds. Physiological and Biotechnological Aspects of Extremophiles. London: Academic Press, 131–136.
    Randolph T G. 1944. Blood studies in allergy: I. The direct counting chamber determination of eosinophils by propylene glycol aqueous stains. Journal of Allergy, 15(2): 89–96, doi: 10.1016/S0021-8707(44)90155-3
    Ruby E G, Wirsen C O, Jannasch H W. 1981. Chemolithotrophic sulfur-oxidizing bacteria from the galapagos rift hydrothermal vents. Applied and Environmental Microbiology, 42(2): 317–324, doi: 10.1128/aem.42.2.317-324.1981
    Teske A, Brinkhoff T, Muyzer G, et al. 2000. Diversity of thiosulfate-oxidizing bacteria from marine sediments and hydrothermal vents. Applied and Environmental Microbiology, 66(8): 3125–3133, doi: 10.1128/AEM.66.8.3125-3133.2000
    Trifinopoulos J, Nguyen L T, von Haeseler A, et al. 2016. W-IQ-TREE: a fast online phylogenetic tool for maximum likelihood analysis. Nucleic Acids Research, 44(W1): W232–W235, doi: 10.1093/nar/gkw256
    Wasmund K, Mussmann M, Loy A. 2017. The life sulfuric: microbial ecology of sulfur cycling in marine sediments. Environmental Microbiology Reports, 9(4): 323–344, doi: 10.1111/1758-2229.12538
    Watanabe T, Kojima H, Umezawa K, et al. 2019. Genomes of neutrophilic sulfur-oxidizing chemolithoautotrophs representing 9 proteobacterial species from 8 genera. Frontiers in Microbiology, 10: 316, doi: 10.3389/fmicb.2019.00316
    Wu Zhengchao, Li Qian P, Ge Zaiming, et al. 2021. Impacts of biogenic polyunsaturated aldehydes on metabolism and community composition of particle-attached bacteria in coastal hypoxia. Biogeosciences, 18(3): 1049–1065, doi: 10.5194/bg-18-1049-2021
    Xie Jianmin, Chen Yuerong, Cai Guanjing, et al. 2023. Tree Visualization By One Table (tvBOT): a web application for visualizing, modifying and annotating phylogenetic trees. Nucleic Acids Research, 51(W1): W587–W592, doi: 10.1093/nar/gkad359
    Zhang Yu, Zhong Xianchun, Xu Wei, et al. 2020. Marinobacter vulgaris sp. nov. , a moderately halophilic bacterium isolated from a marine solar saltern. International Journal of Systematic and Evolutionary Microbiology, 70(1): 450–456, doi: 10.1099/ijsem.0.003774
  • Xu Fei Supplementary material.zip
  • 加载中

Catalog

    通讯作者: 陈斌, bchen63@163.com
    • 1. 

      沈阳化工大学材料科学与工程学院 沈阳 110142

    1. 本站搜索
    2. 百度学术搜索
    3. 万方数据库搜索
    4. CNKI搜索

    Figures(7)  / Tables(1)

    Article Metrics

    Article views (139) PDF downloads(6) Cited by()
    Proportional views
    Related

    /

    DownLoad:  Full-Size Img  PowerPoint
    Return
    Return