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Genome analysis of Pollutimonas subterranea gen. nov., sp. nov. and Pollutimonas nitritireducens sp. nov., isolated from nitrate- and radionuclide-contaminated groundwater, and transfer of several Pusillimonas species into three new genera Allopusillimonas, Neopusillimonas, and Mesopusillimonas

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Abstract

Two facultatively anaerobic, chemoorganoheterotrophic bacterial strains, designated JR1/69-2-13T and JR1/69-3-13T, were isolated from nitrate- and radionuclide-contaminated groundwater (Ozyorsk town, South Urals, Russia). Both strains were found to be motile, Gram-stain negative rod-shaped neutrophilic, psychrotolerant bacteria that grow within the temperature range from 5–10 to 33 °C at 0–3 (0–5)% NaCl (w/v). The major cellular fatty acids were identified as C16:0, C16:1 ω7c, C18:1 ω7c and C17:0 cyclo. The major polar lipids were found to consist of diphosphatidylglycerol, phosphatidylethanolamine, phosphatidylmethylethanolamine, phosphatidylglycerol and unidentified aminophospholipids. The genomic G + C content of strains JR1/69-2-13T and JR1/69-3-13T was determined to be 57.2 and 57.9%, respectively. The 16S rRNA gene sequences of the strains showed high similarity between each other (98.6%) and to members of the genera Pusillimonas (96.8–98.4%) and Candidimonas (97.1–98.0%). The average nucleotide identity and digital DNA–DNA hybridization (dDDH) values among genomes of the new isolates and Pusillimonas and Candidimonas genomes were below 84.5 and 28.8%, respectively, i.e., below the thresholds for species delineation. Based on the phylogenomic, phenotypic and chemotaxonomic characterisation, we propose assignment of strains JR1/69-3-13T (= VKM B-3223T = KCTC 62615T) and JR1/69-2-13T (= VKM B-3222T = KCTC 62614T) to a new genus Pollutimonas as the type strains of two new species, Pollutimonas subterranea gen. nov., sp. nov. and Pollutimonas nitritireducens sp. nov., respectively. As a result of the taxonomic revision of the genus Pusillimonas, three novel genera, Allopusillimonas, Neopusillimonas, and Mesopusillimonas are also proposed; and Candidimonas bauzanensis is reclassified as Pollutimonas bauzanensis comb. nov. Genome analysis of the new isolates suggested molecular mechanisms of their adaptation to an environment highly polluted with nitrate and radionuclides.

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Data availability

The GenBank/EMBL/DDBJ accession numbers of the 16S rRNA gene sequence of strains JR1/69-2-13T and JR1/69-3-13T are MG205613 and MG205614, respectively. The GenBank/EMBL/DDBJ accession numbers of the genomic assemblies of strains JR1/69-2-13T (= VKM B-3222T = KCTC 62614T) and JR1/69-3-13T (= VKM B-3223T = KCTC 62615T) are GCA_002849615.1 (PDNV00000000) and GCA_002849655.1 (PDNW00000000), respectively.

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Acknowledgements

We thank Professor A. Oren from The Hebrew University of Jerusalem (Israel) for his help on the nomenclature of the new species and genera. The authors are grateful N.A. Kostrykina from the Research Center of Biotechnology of the Russian Academy of Sciences, Moscow, Russia, for the help in microscopic studies of the strains. The authors are grateful R.R. Abdullin (present place of work Gemotest Laboratory LLC) for performing environmental studies and isolating the strains. The authors are especially grateful to Professor Iain Sutcliffe from Northumbria University (UK) for editing of the manuscript and for valuable comments. Bioinformatics analysis was performed using computing resources at the SciBear OU (https://sci-bear.com/).

Funding

This research was mainly funded by the Ministry of Science and Higher Education of the Russian Federation.

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Conceptualization: TB, DG and TN; funding acquisition: TN; investigation: TB, DS, TT, AP; DG performed the genomic and phylogenetic analysis; project administration: TN; software: DG and TT: supervision, TN; validation: TB, DG and DS; visualization: TB, DG, and TN; writing original draft, review and editing: DG and TN. All authors have read and approved the final version of the manuscript.

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Correspondence to Tamara N. Nazina.

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The authors declare no conflict of interest. The funders had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript, or in the decision to publish the results.

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This research did not contain any studies with humans or animals performed by any of the authors.

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Babich, T.L., Grouzdev, D.S., Sokolova, D.S. et al. Genome analysis of Pollutimonas subterranea gen. nov., sp. nov. and Pollutimonas nitritireducens sp. nov., isolated from nitrate- and radionuclide-contaminated groundwater, and transfer of several Pusillimonas species into three new genera Allopusillimonas, Neopusillimonas, and Mesopusillimonas. Antonie van Leeuwenhoek 116, 109–127 (2023). https://doi.org/10.1007/s10482-022-01781-1

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