Abstract
A facultatively anaerobic sulfur-oxidizing bacterium, strain skT11T, was isolated from anoxic lake water of a stratified freshwater lake. As electron donor for chemolithoautotrophic growth, strain skT11T oxidized thiosulfate, tetrathionate, and elemental sulfur under nitrate-reducing conditions. Oxygen-dependent growth was observed under microoxic conditions, but not under fully oxygenated conditions. Growth was observed at a temperature range of 5–37 °C, with optimum growth at 28 °C. Strain skT11T grew at a pH range of 5.1–7.5, with optimum growth at pH 6.5–6.9. Heterotrophic growth was not observed. Major components in the cellular fatty acid profile were C16:1 and C16:0. The complete genome of strain skT11T consisted of a circular chromosome with a size of 3.8 Mbp and G + C content of 60.2 mol%. Phylogenetic analysis based on the 16S rRNA gene sequences indicated that the strain skT11T is related to sulfur-oxidizing bacteria of the genera Sulfuricella, Sulfurirhabdus, and Sulfuriferula, with sequence identities of 95.4% or lower. The analysis also indicated that these three genera should be excluded from the family Gallionellaceae, as members of another family. On the basis of its genomic and phenotypic properties, strain skT11T (= DSM 110711 T = NBRC 114323 T) is proposed as the type strain of a new species in a new genus, Sulfurimicrobium lacus gen. nov., sp. nov. In addition, emended descriptions of the families Gallionellaceae and Sulfuricellaceae are proposed to declare that Sulfuricellaceae is not a later synonym of Gallionellaceae.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Boden R, Hutt LP, Rae AW (2017) Reclassification of Thiobacillus aquaesulis (Wood & Kelly, 1995) as Annwoodia aquaesulis gen. nov., comb. nov., transfer of Thiobacillus (Beijerinck, 1904) from the Hydrogenophilales to the Nitrosomonadales, proposal of Hydrogenophilalia class. nov. within the 'Proteobacteria', and four new families within the orders Nitrosomonadales and Rhodocyclales. Int J Syst Evol Microbiol 67:1191–1205. https://doi.org/10.1099/ijsem.0.001927
Chaumeil PA, Mussig AJ, Hugenholtz P, Parks DH (2020) GTDB-Tk: a toolkit to classify genomes with the Genome Taxonomy Database. Bioinfomatics 36:1925–1927. https://doi.org/10.1093/bioinformatics/btz848
Drobner E, Huber H, Rachel R, Stetter KO (1992) Thiobacillus plumbophilus spec. nov., a novel galena and hydrogen oxidizer. Arch Microbiol 157:213–217. https://doi.org/10.1007/BF00245152
Garrity GM, Bell JA, Lilburn T (2005) Order VI. Nitrosomonadales ord. nov. In: Brenner DJ, Krieg NR, Staley JT and Garrity GM (editors). Bergey’s Manual of Systematic Bacteriology, 2nd ed, vol. 2, (The Proteobacteria), part C (The Alpha-, Beta-, Delta-, and Epsilonproteobacteria). New York: Springer. p. 863
Khalifa A, Nakasuji Y, Saka N, Honjo H, Asakawa S, Watanabe T (2018) Ferrigenium kumadai gen. nov., sp. nov., a microaerophilic iron-oxidizing bacterium isolated from a paddy field soil. Int J Syst Evol Microbiol 68:2587–2592. https://doi.org/10.1099/ijsem.0.002882
Kojima H, Fukui M (2010) Sulfuricella denitrificans gen. nov., sp. nov., a sulfur-oxidizing autotroph isolated from a freshwater lake. Int J Syst Evol Microbiol 60:2862–2866. https://doi.org/10.1099/ijs.0.016980-0
Kojima H, Shinohara A, Fukui M (2015) Sulfurifustis variabilis gen. nov., sp. nov., a sulfur oxidizer isolated from a lake, and proposal of Acidiferrobacteraceae fam. nov. and Acidiferrobacterales ord. nov. Int J Syst Evol Microbiol 65:3709–3713. https://doi.org/10.1099/ijsem.0.000479
Kojima H, Watanabe M, Fukui M (2017) Sulfurivermis fontis gen. nov., sp. nov., a sulfur-oxidizing autotroph, and proposal of Thioprofundaceae fam. nov. Int J Syst Evol Microbiol 67:3458–3461. https://doi.org/10.1099/ijsem.0.002137
Kojima H, Mochizuki J, Fukui M (2020) Sulfuriferula nivalis sp. nov. and emended description of Sulfuriferula plumbiphila. Int J Syst Evol Microbiol 70:3273–3277. https://doi.org/10.1099/ijsem.0.004166
Kato S, Krepski S, Chan C, Itoh T, Ohkuma M (2014) Ferriphaselus amnicola gen. nov., sp. nov., a neutrophilic, stalk-forming, iron-oxidizing bacterium isolated from an iron-rich groundwater seep. Int J Syst Evol Microbiol 64:921–925. https://doi.org/10.1099/ijs.0.058487-0
Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: Molecular Evolutionary Genetics Analysis across computing platforms. Mol Biol Evol 35:1547–1549. https://doi.org/10.1093/molbev/msy096
Meyer B, Kuever J (2007) Molecular analysis of the distribution and phylogeny of dissimilatory adenosine-5’-phosphosulfate reductase-encoding genes (aprBA) among sulfur-oxidizing prokaryotes. Microbiology 153:3478–3498. https://doi.org/10.1099/mic.0.2007/008250-0
Parks DH, Chuvochina M, Waite DW, Rinke C, Skarshewski A, Chaumeil PA, Hugenholtz P (2018) A standardized bacterial taxonomy based on genome phylogeny substantially revises the tree of life. Nat Biotechnol 3:996–1004. https://doi.org/10.1038/nbt.4229
Tanizawa Y, Fujisawa T, Nakamura Y (2017) DFAST: a flexible prokaryotic genome annotation pipeline for faster genome publication. Bioinformatics 35:1037–1039. https://doi.org/10.1093/bioinformatics/btx713
Watanabe T, Kojima H, Fukui M (2014) Complete genomes of freshwater sulfur oxidizers Sulfuricella denitrificans skB26 and Sulfuritalea hydrogenivorans sk43H: genetic insights into the sulfur oxidation pathway of betaproteobacteria. Syst Appl Microbiol 37:387–395. https://doi.org/10.1016/j.syapm.2014.05.010
Watanabe T, Kojima H, Fukui M (2015) Sulfuriferula multivorans gen. nov., sp. nov., isolated from a freshwater lake, reclassification of 'Thiobacillus plumbophilus' as Sulfuriferula plumbophilus sp. nov., and description of Sulfuricellaceae fam. nov. and Sulfuricellales ord. nov. Int J Syst Evol Microbiol 65:1504–1508. https://doi.org/10.1099/ijs.0.000129
Watanabe T, Kojima H, Shinohara A, Fukui M (2016a) Sulfurirhabdus autotrophica gen. nov., sp. nov., isolated from a freshwater lake. Int J Syst Evol Microbiol 66:113–117. https://doi.org/10.1099/ijsem.0.000679
Watanabe T, Kojima H, Fukui M (2016b) Sulfuriferula thiophila sp nov., a chemolithoautotrophic sulfur-oxidizing bacterium, and correction of the name Sulfuriferula plumbophilus Watanabe, Kojima and Fukui 2015 to Sulfuriferula plumbiphila corrig. Int J Syst Evol Microbiol 66:2041–2045. https://doi.org/10.1099/ijsem.0.000988
Watanabe T, Kojima H, Fukui M (2016c) Identity of major sulfur-cycle prokaryotes in freshwater lake ecosystems revealed by a comprehensive phylogenetic study of the dissimilatory adenylylsulfate reductase. Sci Rep 6:36262. https://doi.org/10.1038/srep36262
Watanabe T, Kojima H, Umezawa K, Hori C, Takasuka ET et al (2019) Genomes of neutrophilic sulfur-oxidizing chemolithoautotrophs representing 9 proteobacterial species from 8 genera. Front Microbiol 10:316. https://doi.org/10.3389/fmicb.2019.00316
Acknowledgements
We would like to thank A. Shinohara for technical assistance.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflicts of interest
The authors declare that there are no conflicts of interest.
Additional information
Communicated by Erko stackebrandt.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
The GenBank/EMBL/DDBJ accession numbers for the 16S rRNA gene and the complete genome of strain skT11T are LC533074 and AP022853, respectively.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Kojima, H., Kanda, M., Umezawa, K. et al. Sulfurimicrobium lacus gen. nov., sp. nov., a sulfur oxidizer isolated from lake water, and review of the family Sulfuricellaceae to show that it is not a later synonym of Gallionellaceae. Arch Microbiol 203, 317–323 (2021). https://doi.org/10.1007/s00203-020-02029-0
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00203-020-02029-0