Paludisphaera mucosa  sp. nov., a Novel Planctomycete of the Family  Isosphaeraceae  from a Boreal Fen

A. A. Ivanova; Иванова А. А.; D. G. Naumoff; Наумов Д. Г.; I. S. Kulichevskaya; Куличевская И. С.; A. A. Meshcheriakova; Мещерякова А. А.; S. N. Dedysh; Дедыш С. Н.

doi:10.31857/S0026365623600104

Paludisphaera mucosa sp. nov., a Novel Planctomycete of the Family Isosphaeraceae from a Boreal Fen

Authors: Ivanova A.A.¹, Naumoff D.G.¹, Kulichevskaya I.S.¹, Meshcheriakova A.A.¹^,2, Dedysh S.N.¹
Affiliations:
1. Winogradsky Institute of Microbiology, Research Center of Biotechnology, Russian Academy of Sciences
2. Moscow State University, Faculty of Soil Science
Issue: Vol 92, No 4 (2023)
Pages: 347-357
Section: 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

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Abstract

Abstract—Planctomycetes are common inhabitants of northern wetland ecosystems. In this study, a new planctomycete of the genus Paludisphaera, strain Pla2^T, 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 Pla2^T 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’ JC670^T isolated from highland soil of the western Himalayas. With other members of the genus Paludisphaera, “P. rhizosphaerae” JC665^T and P. borealis PX4^T, this similarity was 97.0 and 93.8%, respectively. The genome of strain Pla2^T 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 Pla2^T 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 Pla2^T (=KCTC92668^T = VKM B-3698^T).

Keywords

Planсtomycetes, phylum Planctomycetota, family Isosphaeraceae, genus Paludisphaera, fens, polysaccharide degradation

References

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