Seven New Actinobacterial Species of the Genus  Kribbella  with Unique Cell Wall Glycopolymers, and Emended Description of the Genus  Kribbella

A. N. Avtukh; Автух А. Н.; L. V. Dorofeeva; Дорофеева Л. В.; O. V. Vasilenko; Василенко О. В.; I. P. Starodumova; Стародумова И. П.; N. V. Prisyazhnaya; Присяжная Н. В.; N. E. Suzina; Сузина Н. Е.; A. S. Shashkov; Шашков А. С.; N. V. Potekhina; Потехина Н. В.; E. M. Tul’skaya; Тульская Е. М.; L. M. Baryshnikova; Барышникова Л. М.; E. V. Ariskina; Арискина Е. В.; L. I. Evtushenko; Евтушенко Л. И.

doi:10.31857/S0026365623600220

Seven New Actinobacterial Species of the Genus Kribbella with Unique Cell Wall Glycopolymers, and Emended Description of the Genus Kribbella

Authors: Avtukh A.N.¹, Dorofeeva .V.¹, Vasilenko O.V.¹, Starodumova I.P.¹, Prisyazhnaya N.V.¹, Suzina N.E.¹, Shashkov .S.², Potekhina N.V.³, Tul’skaya E.M.³, Baryshnikova L.M.¹, Ariskina E.V.¹, Evtushenko L.I.¹
Affiliations:
1. All-Russian Collection of Microorganisms (VKM), Skryabin Institute of Biochemistry and Physiology of Microorganisms, Pushchino Scientific Center for Biological Research, Russian Academy of Sciences
2. Zelinsky Institute of Organic Chemistry, Russian Academy of Sciences
3. Faculty of Biology, Moscow State University
Issue: Vol 92, No 5 (2023)
Pages: 453-466
Section: ЭКСПЕРИМЕНТАЛЬНЫЕ СТАТЬИ
URL: https://journals.rcsi.science/0026-3656/article/view/140506
DOI: https://doi.org/10.31857/S0026365623600220
EDN: https://elibrary.ru/JRFOKA
ID: 140506

Cite item

Full Text

Open Access
Restricted Access

Access granted
Restricted Access

Subscription Access

Abstract
About the authors
References
Supplementary files
Statistics

Abstract

Abstract—

Seven actinomycete strains assigned to seven new species of the genus Kribbella were isolated from soils of different regions in Russia. The strains exhibited 98.2–99.3% similarity of the 16S rRNA gene sequences to each other and 96.2–99.7% similarity to the type strains of the known Kribbella species. The evolutionary distances calculated on the basis of concatenated gene sequences (gyrB–rpoB–recA–relA–atpD, 4108 nt) for the studied organisms and type strains of the known species were within the range reported for Kribbella species (0.014–0.101). The dDDH and ANIb values for the strains studied and the type strains of validly described species with available genomes were below the threshold (49.8 and 92.6%, respectively) for prokaryote specie delineation. Members of the putative new species possessed individual phenotypic profiles; some species were found (for the first time in Kribbella) to produce sporangium-like structures, up to 4 μm in diameter. The cell walls of the studied strains contained the teichuronic and/or teichulosonic acids specific for the species or species groups and not described previously for other prokaryotes. The unique branched α-mannan occurred in all studied strains of the genus. Based on the data obtained and the previously published data, the following new species are proposed: Kribbella orskensis sp. nov. (type strain ВКМ Ас-2538^T), Kribbella rubisoli sp. nov. (type strain VKM Aс-2540^T), Kribbella antiqua sp. nov. (type strain VKM Ас-2541^T), Kribbella kalugense sp. nov. (type strain VKM Ас-2570^T), Kribbella steрpae sp. nov. (type strain ВКМ Ас-2572^T), Kribbella pratae sp. nov. (type strain ВКМ Ас-2574^T), and Kribbella voronezhensis sp. nov. (type strain VKM Ас-2575^T) with emended description of the genus Kribbella.

Keywords

genus Kribbella, novel species, genome, chemotaxonomy, cell wall glycopolymers

References

Автух А.Н. Систематика актиномицетов рода Kribbella. Автореферат дис. … канд. биол. наук, 29.06.2012. Пущино: Институт биохимии и физиологии микроорганизмов им. Г.К. Скрябина РАН, 2012. 24 с.
Автух А.Н., Винокурова Н.Г., Арискина Е.В., Дорофеева Л.В., Барышникова Л.М. Состав полярных липидов как хемотаксономический маркер видов рода Kribbella // Вестник Уральской медицинской академической науки. 2011. № 4/1. С. 71.
Методы общей бактериологии. Пер. с англ. / Под ред. Герхардта Ф. и др. М.: Мир, 1984. 264 с.
Manual of Methods for General Bacteriology // Edited by Gerhardt P. American Society for Microbiology, 1981. 524 p.
Потехина Н.В., Шашков А.С., Тульская Е.М., Арискина Е.В., Дорофеева Л.В., Евтушенко Л.И. Галактофуранан клеточной стенки актинобактерий рода Paenarthrobacter // Микробиология. 2021. Т. 90. С. 122–128.
Potekhina N.V., Shashkov A.S., Tul’skaya E.M., Ariskina E.V., Dorofeeva L.V., Evtushenko L.I. Cell wall galactofuranan of the Paenarthrobacter actinobacteria // Microbiology (Moscow). 2021. V. 90. P. 106–111.
Сузина Н.Е., Дуда В.И., Есикова Т.З., Шорохова А.П., Гафаров А.Б., Олейников Р.Р., Акимов В.Н., Абашина Т.Н., Поливцева В.Н., Боронин А.М. Новые ультрамикробактерии из рода Chryseobacterium, штаммы NF4 и NF5 факультативные эпибионты Bacillus subtilis // Микробиология. 2011. Т. 80. С. 529–542.
Suzina N.E., Duda V.I., Esikova T.Z., Shorokhova A.P., Gafarov A.B., Oleinikov R.R., Abashina T.N., Boronin A.M., Akimov V.N., Polivtseva V.N. Novel ultramicrobacteria, strains NF4 and NF5, of the genus Chryseobacterium: facultative epibionts of Bacillus subtilis // Microbiology (Moscow). 2011. V. 80. P. 535–548.
Шашков А.С., Тульская Е.М., Потехина Н.В., Дмитренок А.С., Сенченкова С.Н., Зайчиков В.А., Дорофеева Л.В., Евтушенко Л.И. D-рамнан и пируватсодержащая тейхуроновая кислота клеточной стенки Rathayibacter sp. ВКМ Ac-2759 // Биохимия. 2021. Т. 86. С. 595–606.
Shashkov A.S., Tul’skaya E.M., Potekhina N.V., Dmitrenok A.S., Senchenkova S.N., Zaychikov V.A., Dorofeeva L.V., Evtushenko L.I. D-Rhamnan and pyruvate-containing teichuronic acid from the cell wall of Rathayibacter sp. VKM Ac-2759 // Biochemistry (Moscow). 2021. V. 86. P. 506–516.
Chun J., Oren A., Ventosa A., Christensen H., Arahal D.R., da Costa M.S., Rooney A.P., Yi H., Xu X.-W., De Meyer S., Trujillo M.E. Proposed minimal standards for the use of genome data forthe taxonomy of prokaryotes // Int. J. Syst. Evol. Microbiol. 2018. V. 68. P. 461–466.
Ciufo S., Kannan S., Sharma S., Badretdin A., Clark K., Turner S., Brover S., Schoch C.L., Kimchi A., DiCuccio M. Using average nucleotide identity to improve taxonomic assignments in prokaryotic genomes at the NCBI // Int. J. Syst. Evol. Microbiol. 2018. V. 68. P. 2386–2392.
Curtis S.M., Meyers P.R. Multilocus sequence analysis of the actinobacterial genus Kribbella // Syst. Appl. Microbiol. 2012. V. 35. P. 441–446.
Curtis S.M., Norton I., Everest G.J., Pelser J.G., de Kock M.C., Meyers P.R. Development of a Kribbella-specific isolation medium and description of Kribbella capetownensis sp. nov. and Kribbella speibonae sp. nov., isolated from soil // Antonie van Leeuwenhoek. 2020. V. 113. P. 617–628.
Evtushenko L.I., Krausova V.I. Genus Kribbella Park et al. 1999 emend. Sohn et al. 2003 // Bergey’s Manual of Systematic Bacteriology. V. 5. The Actinobacteria. New York: Springer, 2012. P. 1264–1280.
Everest G.J., Curtis S.M., De Leo F., Urzì C., Meyers P.R. Kribbella albertanoniae sp. nov., isolated from a Roman catacomb, and emended description of the genus Kribbella // Int. J. Syst. Evol. Microbiol. 2013. V. 63. P. 3591–3596.
Guo L., Zhao J., Liu C., Han C., Bai L., Sun P., Li J., Wang X., Xiang W. Kribbella qitaiheensis sp. nov., a novel actinomycete isolated from soil // Antonie van Leeuwenhoek. 2015. V. 6. P. 1533–1539.
Kimura M. A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences // J. Mol. Evol. 1980. V. 16. P. 111–120.
Kirby B.M., Le Roes M., Meyers P.R. Kribbella karoonensis sp. nov. and Kribbella swartbergensis sp. nov., isolated from soil from the Western Cape, South Africa // Int. J. Syst. Evol. Microbiol. 2006. V. 56. P. 1097–1101.
Kirby B.M., Everest G.J., Meyers P.R. Phylogenetic analysis of the genus Kribbella based on the gyrB gene: proposal of a gyrB-sequence threshold for species delineation in the genus Kribbella // Antonie van Leeuwenhoek. 2010. V. 97. P. 131–142.
Kumar S., Stecher G., Tamura K. MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets // Mol. Biol. Evol. 2016. V. 33. P. 1870–1874.
Lane D.J. 16S/23S rRNA sequencing // Nucleic Acid Techniques in Bacterial Systematics / Eds. Stackebrandt E., Goodfellow M. Chichester: Wiley, 1991. P. 115–175.
Lee S.D., Kang S.O., Hah Y.C. Hongia gen. nov., a new genus of the order Actinomycetales // Int. J. Syst. Evol. Microbiol. 2000. V. 50. P. 191–199.
Meier-Kolthoff J.P., Auch A.F., Klenk H.-P., Göker M. Genome sequence-based species delimitation with confidence intervals and improved distance functions // BMC Bioinform. 2013. V. 14. P. 60.
Meyers P. Genus Kribbella // Bergey’s Manual of Systematic Bacteriology / Ed. Carro L. Wiley: 2021. https://doi.org/10.1002/9781118960608.gbm00157.pub2
Naumova I.B., Shashkov A.S., Tul’skaya E.M., Streshin-skaya G.M., Kozlova Y.I., Potekhina N.V., Evtushenko L.I., Stackebrandt E. Cell wall teichoic acids: structural diversity, species specificity in the genus Nocardiopsis, and chemotaxonomic perspective // FEMS Microbiol. Rev. 2001. V. 25. P. 269–283.
Nouioui I., Carro L., Garcia-Lopez M., Meier-Kolthoff J.P., Woyke T., Kyrpides N.C., Pukall R., Klenk H.P., Goodfellow M., Göker M. Genome-based taxonomic classification of the phylum Actinobacteria // Front. Microbiol. 2018. V. 9. https://doi.org/10.3389/fmicb.2018.02007
Olson R.D., Assaf R., Brettin T., Conrad N., Cucinell C., Davis J.J., Dempsey D.M., Dickerman A., Dietrich E.M., Kenyon R.W., Kuscuoglu M., Lefkowitz E.J., Lu J., Machi D., Macken C., Mao C., Niewiadomska A., Nguyen M., Olsen G.J., Overbeek J.C., Parrello B., Parrello V., Porter J.S., Pusch G.D., Shukla M., Singh I., Stewart L., Tan G., Thomas C., VanOeffelen M., Vonstein V., Wallace Z.S., Warren A.S., Wattam A.R., Xia F., Yoo H., Zhang Y., Zmasek C.M., Scheuermann R.H., Stevens R.L. Introducing the Bacterial and Viral Bioinformatics Resource Center (BV-BRC): a resource combining PATRIC, IRD and ViPR // Nucleic Acids Res. 2023. V. 51. I. D. P. D678–D689.
Ozdemir-Kocak F., Saygin H., Saricaoglu S., Cetin D., Guven K., Spröer C., Schumann P., Klenk H.P., Sahin N., Isik K. Kribbella soli sp. nov., isolated from soil // Antonie van Leeuwenhoek. 2017. V. 110. P. 641–649.
Park Y.-H., Yoon J.-H., Shin Y.K., Suzuki K.-I., Kudo T., Seino A., Kim H.-J., Lee J.-S., Lee S.T. Classification of “Nocardioides fulvus” IFO (now NBRC) 14399 and Nocardioides sp. ATCC 39419 in Kribbella gen. nov., as Kribbella flavida sp. nov. and Kribbella sandramycini sp. nov. // Int. J. Syst. Bacteriol. 1999. V. 49. P. 743–752.
Richter M., Rosselló-Móra R., Glöckner F.O., Peplies J. JSpeciesWS: a web server for prokaryotic species circumscription based on pairwise genome comparison // Bioinformatics. 2015. V. 32. P. 929–931.
Saygin H., Ay H., Guven K., Sahin N. Kribbella turkmenica sp. nov., isolated from the Karakum Desert // Int. J. Syst. Evol. Microbiol. 2019. V. 69. P. 2533–2540.
Shashkov A.S., Tul’skaya E.M., Streshinskaya G.M., Senchenkova S.N., Avtukh A.N., Evtushenko L.I. New cell wall glycopolymers of the representatives of the genus Kribbella // Carb. Res. 2009. V. 344. P. 2255–2262.
Shirling E.B., Gottlieb D. Methods for characterization of Streptomyces species // Int. J. Syst. Bacteriol. 1966. V. 16. P. 313.
Sohn K., Hong S.G., Bae K.S., Chun J. Transfer of Hongia koreensis Lee et al. 2000 to the genus Kribbella Park et al. 1999 as Kribbella koreensis comb. nov. // Int. J. Syst. Evol. Microbiol. 2003. V. 53. P. 1005–1007.
Song W., Duan L., Zhao J., Jiang S., Guo X., Xiang W., Wang X. Kribbella monticola sp. nov., a novel actinomycete isolated from soil // Int. J. Syst. Evol. Microbiol. 2018. V. 68. P. 3441–3446.
Sorokin D.Y., Khijniak T.V., Zakharycheva A.P., Elcheninov A.G., Hahnke R.L., Boueva O.V., Ariskina E.V., Bunk B., Kublanov I.V., Evtushenko L.I. Natronoglycomyces albus gen. nov., sp. nov., a haloalkaliphilic actinobacterium from a soda solonchak soil // Int. J. Syst. Evol. Microbiol. 2021. V. 71. Art. 004804.
Tul’skaya E.M., Streshinskaya G.M., Shashkov A.S., Senchenkova S.N., Avtukh A.N., Baryshnikova L.M., Evtushenko L.I. Novel teichulosonic acid from cell walls of some representatives of the genus Kribbella // Carb. Res. 2011. V. 346. P. 2045–2051.
Wilson K. Preparation of genomic DNA from bacteria // Current Protocols in Molecular Biology. New York: Wiley, 1997. P. 241–245.
Yoon S.H., Ha S.M., Kwon S., Lim J., Kim Y., Seo H., Chun J. Introducing EzBioCloud: a taxonomically united database of 16S rRNA and whole genome assemblies // Int. J. Syst. Evol. Microbiol. 2017. V. 67. P. 1613–1617.
Zhao J., Duan L., Qian L., Cao P., Tian Y., Ju H., Xiang W., Wang X. Kribbella jiaozuonensis sp. nov., a novel actinomycete isolated from soil // Int. J. Syst. Evol. Microbiol. 2019. V. 69. P. 3500–3507.