Paludisphaera mucosa sp. nov., a Novel Planctomycete of the Family Isosphaeraceae from a Boreal Fen
- Autores: Ivanova A.1, Naumoff D.1, Kulichevskaya I.1, Meshcheriakova A.1,2, Dedysh S.1
-
Afiliações:
- Winogradsky Institute of Microbiology, Research Center of Biotechnology, Russian Academy of Sciences
- Moscow State University, Faculty of Soil Science
- Edição: Volume 92, Nº 4 (2023)
- Páginas: 347-357
- Seção: ЭКСПЕРИМЕНТАЛЬНЫЕ СТАТЬИ
- URL: https://journals.rcsi.science/0026-3656/article/view/138204
- DOI: https://doi.org/10.31857/S0026365623600104
- EDN: https://elibrary.ru/RKYILM
- ID: 138204
Citar
Resumo
Abstract—Planctomycetes are common inhabitants of northern wetland ecosystems. In this study, a new planctomycete of the genus Paludisphaera, strain Pla2T, was isolated from a boreal fen in Russia. The novel isolate was represented by nonmotile, pink-pigmented, spherical cells that multiplied by budding and occurred singly or were assembled in small aggregates. Strain Pla2T was a chemoorganotrophic, psychrotolerant mesophile with a growth optimum at pH 5.5‒6 and 15‒20°C. The preferred growth substrates were polysaccharides, including xylan, xanthan gum, and phytagel, as well as some sugars. The 16S rRNA gene sequence of strain Pla2T displayed the highest similarity (97.9%) to that of ‘Paludisphaera soli’ JC670T isolated from highland soil of the western Himalayas. With other members of the genus Paludisphaera, “P. rhizosphaerae” JC665T and P. borealis PX4T, this similarity was 97.0 and 93.8%, respectively. The genome of strain Pla2T was 8.21 Mb in size and contained about 6500 protein-coding genes and 3 copies of the rRNA operon. The DNA G + C content was 67 mol %. The average nucleotide identity between the genome sequence of strain Pla2T and those of previously described members of the genus Paludisphaera was between 79.4 and 82.6%. This genotypic distance as well as several phenotypic differences allowed classifying the new planctomycete from a fen as representing a novel species of the genus Paludisphaera, Paludisphaera mucosa sp. nov. with the type strain Pla2T (=KCTC92668T = VKM B-3698T).
Sobre autores
A. Ivanova
Winogradsky Institute of Microbiology, Research Center of Biotechnology, Russian Academy of Sciences
Autor responsável pela correspondência
Email: ivanovastasja@gmail.com
Russia, 119071, Moscow
D. Naumoff
Winogradsky Institute of Microbiology, Research Center of Biotechnology, Russian Academy of Sciences
Email: ivanovastasja@gmail.com
Russia, 119071, Moscow
I. Kulichevskaya
Winogradsky Institute of Microbiology, Research Center of Biotechnology, Russian Academy of Sciences
Email: ivanovastasja@gmail.com
Russia, 119071, Moscow
A. Meshcheriakova
Winogradsky Institute of Microbiology, Research Center of Biotechnology, Russian Academy of Sciences; Moscow State University, Faculty of Soil Science
Email: ivanovastasja@gmail.com
Russia, 119071, Moscow; Russia, 119991, Moscow
S. Dedysh
Winogradsky Institute of Microbiology, Research Center of Biotechnology, Russian Academy of Sciences
Email: ivanovastasja@gmail.com
Russia, 119071, Moscow
Bibliografia
- Наумов Д.Г. Филогенетический анализ α-галактозидаз семейства GH27 // Мол. биология. 2004. Т. 38. С. 463–476.
- Naumoff D.G. Phylogenetic analysis of α-galactosidases of the GH27 family // Mol. Biol. (Moscow). 2004. V. 38. P. 388–399. https://doi.org/10.1023/B:MBIL.0000032210.97006.de
- Наумов Д.Г. Иерархическая классификация гликозил-гидролаз // Биохимия. 2011. Т. 76. С. 764–780.
- Naumoff D.G. Hierarchical classification of glycoside hydrolases // Biochemistry (Moscow). 2011. V. 76. P. 622–635. https://doi.org/10.1134/S0006297911060022
- Наумов Д.Г. Семейство GH10 гликозилгидролаз: структура и эволюционные связи // Мол. биология. 2016. Т. 50. С. 151–160.
- Naumoff D.G. GH10 family of glycoside hydrolases: structure and evolutionary connections // Mol. Biol. (Moscow). 2016. V. 50. P. 132–140. https://doi.org/10.1134/S0026893315060205
- Наумов Д.Г., Куличевская И.С., Дедыш С.Н. Генетические детерминанты утилизации ксилана у планктомицета класса Phycisphaerae, Humisphaera borealis M1803T // Микробиология. 2022. Т. 91. С. 300–311.
- Naumoff D.G., Kulichevskaya I.S., Dedysh S.N. Genetic determinants of xylane utilization in Humisphaera borealis M1803T, a planctomycete of the class Phycisphaerae // Microbiology (Moscow). 2022. V. 91. P. 249–258. https://doi.org/10.1134/S002626172230004X
- Bondoso J., Albuquerque L., Nobre M.F., Lobo-da-Cunha A., da Costa M.S., Lage O.M. Aquisphaera giovannonii gen. nov., sp. nov., a planctomycete isolated from a freshwater aquarium // Int. J. Syst. Evol. Microbiol. 2011. V. 61. P. 2844–2850. https://doi.org/10.1099/ijs.0.027474-0
- Chaumeil P.-A., Mussig A.J., Hugenholtz P., Parks D.H. GTDB-Tk: a toolkit to classify genomes with the Genome Taxonomy Database // Bioinformatics. 2020. V. 36. P. 1925–1927. https://doi.org/10.1093/bioinformatics/btz848
- Chun J., Oren A., Ventosa A., Christensen H., Arahal D.R., da Costa M.S. et al. Proposed minimal standards for the use of genome data for the taxonomy of prokaryotes // Int. J. Syst. Evol. Microbiol. 2018. V. 68. P. 461–466. https://doi.org/10.1099/ijsem.0.002516
- Dedysh S.N., Beletsky A.V., Ivanova A.A., Kulichevskaya I.S., Suzina N.E., Philippov D.A. et al. Wide distribution of Phycisphaera-like planctomycetes from WD2101 soil group in peatlands and genome analysis of the first cultivated representative // Environ. Microbiol. 2020. V. 23. P. 1510–1526. https://doi.org/10.1111/1462-2920.15360
- Dedysh S.N., Ivanova A.A. Planctomycetes in boreal and subarctic wetlands: diversity patterns and potential ecological functions // FEMS Microbiol. Ecol. 2019. V. 95. Art. fiy227. https://doi.org/10.1093/femsec/fiy227
- Donadio S., Monciardini P., Sosio M. Polyketide synthases and nonribosomal peptide synthetases: the emerging view from bacterial genomics // Nat. Prod. Rep. 2007. V. 24. P. 1073–1109. https://doi.org/10.1039/b514050c
- Drula E., Garron M.-L., Dogan S., Lombard V., Henrissat B., Terrapon N. The carbohydrate-active enzyme database: functions and literature // Nucl. Acids Res. 2022. № Database issue (50). P. D571–D577. https://doi.org/10.1093/nar/gkab1045
- Ferrer L., Mindt M., Suarez-Diez M., Jilg T., Zagorščak M., Lee J.H. et al. Fermentative indole production via bacterial tryptophan synthase alpha subunit and plant indole-3-glycerol phosphate lyase enzymes // J. Agric. Food Chem. 2022. V. 70. P. 5634–5645. https://doi.org/10.1021/acs.jafc.2c01042
- Giovannoni S.J., Schabtach E., Castenholz R.W. Isosphaera pallida, gen. and comb. nov., a gliding, budding eubacterium from hot springs // Arch. Microbiol. 1987. V. 147. P. 276–284. https://doi.org/10.1007/BF00463488
- Göker M., Cleland D., Saunders E., Lapidus A., Nolan M., Lucas S. et al. Complete genome sequence of Isosphaera pallida type strain (IS1B) // Stand. Genom. Sci. 2011. V. 4. P. 63–71. https://doi.org/10.4056/sigs.1533840
- Helfrich E.J.N., Lin G.M., Voigt C.A., Clardy J. Bacterial terpene biosynthesis: challenges and opportunities for pathway engineering // Beilstein J. Org. Chem. 2019. V. 15. P. 2889–2906. https://doi.org/10.3762/bjoc.15.283
- Ivanova A.A., Naumoff D.G., Miroshnikov K.K., Liesack W., Dedysh S.N. Comparative genomics of four Isosphaeraceae planctomycetes: a common pool of plasmids and glycoside hydrolase genes shared by Paludisphaera borealis PX4T, Isosphaera pallida IS1BT, Singulisphaera acidiphila DSM 18658T, and strain SH-PL62 // Front. Microbiol. 2017. V. 8. P. 412. https://doi.org/10.3389/fmicb.2017.00412
- Kanehisa M., Sato Y., Morishima K. BlastKOALA and GhostKOALA: KEGG tools for functional characterization of genome and metagenome sequences // J. Mol. Biol. 2016. V. 428. P. 726–731. https://doi.org/10.1016/j.jmb.2015.11.006
- Kaushik R., Sharma M., Gaurav K., Jagadeeshwari U., Shabbir A., Sasikala C. et al. Paludisphaera soli sp. nov., a new member of the family Isosphaeraceae isolated from high altitude soil in the Western Himalaya // Antonie van Leeuwenhoek. 2020. V. 113. P. 1663–1674. https://doi.org/10.1007/s10482-020-01471-w
- Kovaleva O.L., Elcheninov A.G., Toshchakov S.V., Novikov A.A., Bonch-Osmolovskaya E.A., Kublanov I.V. Tautonia sociabilis gen. nov., sp. nov., a novel thermotolerant planctomycete, isolated from a 4000 m deep subterranean habitat // Int. J. Syst. Evol. Microbiol. 2019. V. 69. P. 2299–2304. https://doi.org/10.1099/ijsem.0.003467
- Kulichevskaya I.S., Ivanova A.A., Detkova E.N., Rijpstra W.I.C., Sinninghe Damsté J.S., Dedysh S.N. Tundrisphaera lichenicola gen. nov., sp. nov., a psychrotolerant representative of the family Isosphaeraceae from lichen-dominated tundra soils // Int. J. Syst. Evol. Microbiol. 2017. V. 67. P. 3583–3589. https://doi.org/10.1099/ijsem.0.002172
- Kulichevskaya I.S., Ivanova A.A., Suzina N.E., Rijpstra W.I.C., Damsté J.S.S., Dedysh S.N. Paludisphaera borealis gen. nov., sp. nov., a hydrolytic planctomycete from northern wetlands, and the proposal of Isosphaeraceae fam. nov. // Int. J. Syst. Evol. Microbiol. 2016. V. 66. P. 837–844. https://doi.org/10.1099/ijsem.0.000799
- Kulichevskaya I.S., Ivanova A.O., Baulina O.I., Bodelier P.L.E., Damsté J.S.S., Dedysh S.N. Singulisphaera acidiphila gen. nov., sp. nov., a non-filamentous, Isosphaera-like planctomycete from acidic northen wetlands // Int. J. Syst. Evol. Microbiol. 2008. V. 58. P. 1186–1193. https://doi.org/10.1099/ijs.0.65593-0
- Kumar S., Stecher G., Li M., Knyaz C., Tamura K. MEGA X : molecular evolutionary genetics analysis across computing platforms // Mol. Biol. Evol. 2018. V. 35. P. 1547–1549. https://doi.org/10.1093/molbev/msy096
- Lane D.J. 16S/23S rRNA sequencing // Nucleic Acid Techniques in Bacterial Systematic / Eds. Stackebrandt E., Goodfellow M., New York: John Wiley & Sons, 1991. P. 115–175.
- Lhingjakim K.L., Smita N., Kumar G., Jagadeeshwari U., Ahamad S., Sasikala C. et al. Paludisphaera rhizosphaereae sp. nov., a new member of the family Isosphaeraceae, isolated from the rhizosphere soil of Erianthus ravennae // Antonie van Leeuwenhoek. 2022. V. 115. P. 1073–1084. https://doi.org/10.1007/s10482-022-01758-0
- Medema M.H., Blin K., Cimermancic P., De Jager V., Zakrzewski P., Fischbach M.A. et al. AntiSMASH: rapid identification, annotation and analysis of secondary metabolite biosynthesis gene clusters in bacterial and fungal genome sequences // Nucl. Acids Res. 2011. V. 39 (Web Server issue) P. W339–W346. https://doi.org/10.1093/nar/gkr466
- Moore E.K., Villanueva L., Hopmans E.C., Rijpstra W.I.C., Mets A., Dedysh S.N. et al. Abundant trimethylornithine lipids and specific gene sequences are indicative of planctomycete importance at the oxic/anoxic interface in Sphagnum-dominated northern wetlands // Appl. Environ. Microbiol. 2015. V. 81. P. 6333–6344. https://doi.org/10.1128/AEM.00324-15
- Naumoff D.G. β-Fructosidase superfamily: homology with some α-L-arabinases and β-D-xylosidases // Proteins. 2001. V. 42. P. 66–67. https://doi.org/10.1002/1097-0134(20010101)42:1<66::AID- PROT70>3.0.CO;2-4
- Seemann T. Prokka: rapid prokaryotic genome annotation // Bioinformatics. 2014. V. 30. P. 2068–2069. https://doi.org/10.1093/bioinformatics/btu153
- Serkebaeva Y.M., Kim Y., Liesack W., Dedysh S.N. Pyrosequencing-based assessment of the bacteria diversity in surface and subsurface peat layers of a northern wetland, with focus on poorly studied phyla and candidate divisions // PloS One. 2013. V. 8. P. e63994. https://doi.org/10.1371/journal.pone.0063994
- Staley J.T., Fuerst J.A., Giovannoni S., Schlesner H. The order Planctomycetales and the genera Planctomyces, Pirellula, Gemmata, and Isosphaera // The Prokaryotes / Eds. Balows A. et al. New York, NY: Springer New York, 1992. P. 3710–3731.
- Wick R.R., Judd L.M., Gorrie C.L., Holt K.E. Unicycler: resolving bacterial genome assemblies from short and long sequencing reads // PLoS Comput. Biol. 2017. V. 13. P. e1005595. https://doi.org/10.1371/journal.pcbi.1005595
- Wiegand S., Jogler M., Jogler C. On the maverick Planctomycetes // FEMS Microbiol. Rev. 2018. V. 42. P. 739–760. https://doi.org/10.1002/adsc.201