Ancylobacter crimeensis  sp. nov., a New Species of Aerobic Methylotrophic Bacteria Isolated from Oak Phyllosphere

A. A. Belova; Белова А. А.; E. N. Kaparullina; Капаруллина Е. Н.; N. V. Agafonova; Агафонова Н. В.; D. S. Grouzdev; Груздев Д. С.; D. S. Kopitsyn; Копицын Д. С.; А. V. Machulin; Мачулин А. В.; N. V. Doronina; Доронина Н. В.

doi:10.31857/S0026365623600128

Ancylobacter crimeensis sp. nov., a New Species of Aerobic Methylotrophic Bacteria Isolated from Oak Phyllosphere

Authors: Belova A.A.¹, Kaparullina E.N.¹, Agafonova N.V.¹, Grouzdev D.S.², Kopitsyn D.S.³, Machulin .V.¹, Doronina N.V.¹
Affiliations:
1. Skryabin Institute of Biochemistry and Physiology of Microorganisms, Russian Academy of Sciences, Federal Research Center “Pushchino Scientific Center for Biological Research of the Russian Academy of Sciences”
2. SciBear OU
3. Gubkin University
Issue: Vol 92, No 5 (2023)
Pages: 441-452
Section: EXPERIMENTAL ARTICLES
URL: https://journals.rcsi.science/0026-3656/article/view/140505
DOI: https://doi.org/10.31857/S0026365623600128
EDN: https://elibrary.ru/YGLVXG
ID: 140505

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Abstract
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Abstract

Abstract—

A new facultative methylotroph, strain 6x-1^T, was isolated from the phyllosphere of oak (Quercus pubescens Willd.) on the medium with methanol. Cells were aerobic, gram-negative, not-spore-forming, non-motile short ovoids rods reproducing by binary fission. Growth optimum was at 25‒29°C and pH 7.0‒7.5; growth was inhibited by 1.5% NaCl. Predominant fatty acids were C_18:1ω7c and C_19:0cyclo. Predominant phospholipids were phosphatidylethanolamine, phosphatidylmonomethylethanolamine, and diphosphatidylglycerol. Tha major ubiquinone was Q₁₀. The 16S rRNA gene sequence of strain 6x-1^T exhibited the highest similarity to those of members of the genus Ancylobacter (97.0‒97.4%). Genome analysis of strain 6x-1^T and most closely related Ancylobacter strains revealed that the values of ANI (80.7‒83.5%), dDDH (22.4‒23.3%), AAI (72.0‒78.0%), and POCP (62.0‒69.0%) were below the recommended threshold values for prokaryotic species. Genome size of strain 6x-1^T was 4.29 × 10⁶ Mb, and G + C content was 67.3%. According to the results of phylogenetic, phylogenomic, phenotypic, and chemotaxonomic analysis, strain 6x-1^T (=VKM В-3256^T = ССUG 72401^T) represents a new species of genus Ancylobacter, for which the name Ancylobacter crimeensis sp. nov. is proposed.

Keywords

Ancylobacter crimeensis sp. nov., facultative methylotroph, new species, methanol

References

Агафонова Н.В., Капаруллина Е.Н., Доронина Н.В., Троценко Ю.А. Фосфатсолюбилизирующая активность аэробных метилобактерий // Микробиология. 2014. Т. 83. С. 28‒32.
Agafonova N.V., Kaparullina E.N., Doronina N.V., Trotsenko Y.A. Phosphatesolubilizing activity of aerobic methylobacteria // Microbiology (Moscow). 2013. V. 82. P. 864–867.
Порошина М.Н., Доронина Н.В., Капаруллина Е.Н., Ковалевская Н.П., Троценко Ю.А. Галофильные и галотолерантные аэробные метилобактерии из техногенных биотопов // Микробиология. 2013. Т. 84. С. 473‒482.
Poroshina M.N., Doronina N.V., Kaparullina E.N., Kovalevskaya N.P., Trotsenko Y.A. Halophilic and halotolerant aerobic methylobacteria from the technogenic Solikamsk biotopes // Microbiology (Moscow). 2013. V. 82. P. 490‒498.
Чемодурова А.А., Капаруллина Е.Н., Мачулин А.В., Spröer C., Lang E., Доронина Н.В. Ancylobacter lacus sp. nov. и Ancylobacter plantiphilus sp. nov. ‒ новые аэробные факультативно-метилотрофные бактерии, использующие метанол // Микробиология. 2020. Т. 89. С. 42‒51.
Chemodurova A.A., Kaparullina E.N., Machulin A.V., Spröer C., Lang E., Doronina N.V. Ancylobacter lacus sp. nov. and Ancylobacter plantiphilus sp. nov. ‒ novel aerobic facultative methylotrophic bacteria // Microbiology (Moscow). 2020. V. 89. P. 35‒43.
Чемодурова А.А., Решетников А.С., Агафонова Н.В., Доронина Н.В. Гены, кодирующие НАД+-зависимые формиатдегидрогеназы, в таксономии аэробных метилотрофных бактерий рода Ancylobacter // Микробиология. 2023. Т. 92. С. 98‒102.
Chemodurova A.A., Reshetnikov A.S., Agafonova N.V., Doronina N.V. Genes of NAD+-dependent formate dehydrogenases in taxonomy of aerobic methylotrophic bacteria of the genus Ancylobacter // Microbiology(Moscow). 2022. V. 91. P. 834‒838.
Agafonova N., Kaparullina E., Trotsenko Y., Doronina N. Ancylobacter sonchi sp. nov., a novel methylotrophic bacterium from roots of Sonchus arvensis L. // Int. J. Syst. Evol. Microbiol. 2017. V. 67. P. 4552‒4558.
Aziz R.K., Bartels D., Best A.A., De Jongh M., Disz T., Edwards R.A., Zagnitko O. The RAST Server: rapid annotations using subsystems technology // BMC Genomics. 2008. V. 9. P. 1‒15.
Banik A., Mukhopadhaya S.K., Dangar T.K. Characterization of N2-fixing plant growth promoting endophytic and epiphytic bacterial community of Indian cultivated and wild rice (Oryza spp.) genotypes // Planta. 2016. V. 243. P. 799–812.
Bankevich A., Nurk S., Antipov D., Gurevich A., Dvorkin M., Kulikov A., Lesin V., Nikolenko S., Pham S., Prjibelski A., Pyshkin A., Sirotkin A., Vyahhi N., Tesler G., Alekseyev M., Pevzner P. SPAdes: A new genome assembly algorithm and its applications to single-cell sequencing // J. Comput. Biol. 2012. V. 19. P. 455‒477.
Bolger A.M., Lohse M., Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data // Bioinformatics. 2014. V. 30. P. 2114‒2120.
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.
Chun J., Oren A., Ventosa A., Christensen H., Arahal D.R., daCosta 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 for the taxonomy of prokaryotes // Int. J. Syst. Evol. Microbiol. 2018. V. 68. P. 461–466.
Dimise E.J., Widboom P.F., Bruner S.D. Structure elucidation and biosynthesis of fuscachelins, peptide siderophores from the moderate thermophile Thermobifida fusca // Proc. Natl. Acad. Sci. USA. 2008. V. 105. P. 15311‒15316.
Doronina N.V., Chemodurova A.A., Grouzdev D.S., Koziaeva V.V., Shi W., Wu L., Kaparullina E.N. Ancylobacter moscoviensis sp. nov., facultatively methylotrophic bacteria from activated sludge and the reclassification of Starkeya novella (Starkey 1934) Kelly et al. 2000 as Ancylobacter novellus comb. nov., Starkeya koreensis Im et al. 2006 as Ancylobacter koreensis comb. nov., Angulomicrobium tetraedrale Vasil’eva et al. 1986 as Ancylobacter tetraedralis comb. nov., Angulomicrobium ammanitiforme Fritz et al. 2004 as Ancylobacter ammanitiformis comb. nov. // Antonie van Leeuwenhoek. 2023. V. 116. P. 153‒170.
Doronina N.V., Gogleva A.A., Trotsenko Y.A. Methylophilus glucosoxydans sp. nov., a restricted facultative methylotroph from rice rhizosphere // Int. J. Syst. Evol. Microbiol. 2012. V. 62. P. 196‒201.
Firsova J., Doronina N., Lang E., Spröer C., Vuilleumier S., Trotsenko Y. Ancylobacter dichloromethanicus sp. nov. ‒ a new aerobic facultatively methylotrophic bacterium utilizing dichloromethane // Syst. Appl. Microbiol. 2009. V. 32. P. 227–232.
Gordon S.A., Weber R.P. Colorimetric estimation of indoleacetic acid // Plant Physiol. 1951. V. 26. P. 192–195.
Härtig C. Rapid identification of fatty acid methyl esters using a multidimensional gas chromatography–mass spectrometry database // J. Chromatogr. A. 2008. V. 1177. P. 159‒169.
Hoang D.T., Chernomor O., von Haeseler A., Minh B.Q., Vinh L.S. UFBoot2: improving the ultrafast bootstrap approximation // Mol. Biol. Evol. 2018. V. 35. P. 518–522.
Kalyaanamoorthy S., Minh B.Q., Wong T.K.F., von Haeseler A., Jermiin L.S. ModelFinder: Fast model selection for accurate phylogenetic estimates // Nature Methods. 2017. V. 14. P. 587–589.
Kaparullina E.N., Trotsenko Yu.A., Doronina N.V. Methylobacillus methanolivorans sp. nov., a novel non-pigmented obligately methylotrophic bacterium // Int. J. Syst. Evol. Microbiol. 2017. V. 67. P. 425‒431.
Kim M., Oh H.-S., Park S.-C., Chun J. Towards a taxonomic coherence between average nucleotide identity and 16S rRNA gene sequence similarity for species demarcation of prokaryotes // Int. J. Syst. Evol. Microbiol. 2014. V. 64. P. 346–351.
Konstantinidis K.T., Roselló-Móra R., Amann R. Uncultivated microbes in need of their own taxonomy // ISME J. 2017. V. 11. P. 2399–2406.
Lane D.J. 16S/23S rRNA sequencing // Nucleic acid Techniques in Bacterial Systematics / Eds. Stackebrandt E., Goodfellow M. Chichester: John Wiley and Sons, 1991. P. 115–175.
Lang E., Swiderski J., Stackebrandt E., Schumann P., Spröer C., Sahin N. Description of Ancylobacter oerskovii sp. nov. and two additional strains of Ancylobacter polymorphus // Int. J. Syst. Evol. Microbiol. 2008. V. 58. P. 1997–2002.
Lu P., Jin L., Liang B., Zhang J., Li S., Feng Z., Huang X. Study of biochemical pathway and enzyme involved in metsulfuronmethyl degradation by Ancylobacter sp. XJ-412-1 isolated from soil // Curr. Microbiol. 2011. V. 62. P. 1718–1725.
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. Art. 60.
Nguyen L.T., Schmidt H.A., von Haeseler A., Minh B.Q. IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies // Mol. Biol. Evol. 2015. V. 32. P. 268–274.
Nie W., Zheng X., Wang S., Ahmad I., Zhu B. Genome resource of Ancylobacter pratisalsi E130T: a novel plant-growth-promoting bacterium isolated from the rhizosphere // Phytopathol. 2022. V. 112. P. 729–731.
Ørskov J. Beschreibung eines neuen Mikroben, Microcyclus aquaticus, mit eigentuemlicher Morphologie // Zentralbl Bakteriol Parasitenkd Infektionskr Hyg Abt I. 1928. V. 107. P. 180–184 (in German).
Raj H.D. Proposal of Ancylobacter gen. nov. as a substitute for the bacterial genus Microcyclus Ørskov 1928 // Int. J. Syst. Evol. Microbiol. 1983. V. 33. P. 397–398.
Schwyn B., Neilands J.B. Universal chemical assay for the detection and determination of siderophores // Anal. Biochem. 1987. V. 160. P. 47–56.
Slobodkina G.B., Merkel A.Y., Novikov A.A., Bonch-Osmolovskaya E.A., Slobodkin A.I. Pelomicrobium methylotrophicum gen. nov., sp. nov. a moderately thermophilic, facultatively anaerobic, lithoautotrophic and methylotrophic bacterium isolated from a terrestrial mud volcano // Extremophiles. 2020. V. 24. P. 177–185.
Staley J.T., Jenkins C., Konopka A.E. Ancylobacter // Bergey’s Manual of Systematics of Archaea and Bacteria / Eds. Trujillo M.E., Dedysh S., DeVos P., Hedlund B., Kämpfer P., Rainey F.A., Whitman W.B., 2015. https://doi.org/10.1002/9781118960608.gbm00811
Suarez Ch., Ratering S., Spröer J., Schnell S. Ancylobacter pratisalsi sp. nov. with plant growth promotion abilities from the rhizosphere of Plantago winteri Wirtg. // Int. J. Syst. Evol. Microbiol. 2017. V. 67. P. 4500‒4506.
Tamura K., Peterson D., Peterson N., Stecher G., Nei M., Kumar S. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods // Mol. Biol. Evol. 2011. V. 28. P. 2731–2739.
Tatusova T., DiCuccio M., Badretdin A., Chetvernin V., Nawrocki E.P. NCBI prokaryotic genome annotation pipeline // Nucl. Acids Res. 2016. V. 44. P. 6614–6624.
Thompson J.D., Gibson T.J., Plewniak F., Jeanmougin F., Higgins D.G. The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools // Nucl. Acids Res. 1997. V. 25. P. 4876–4882.
van den Wijngaard A.J., Prins J., Smal A.J., Janssen D.B. Degradation of 2-chloroethylvinylether by Ancylobacter aquaticus AD25 and AD27 // Appl. Environ. Microbiol. 1993. V. 59. P. 2777–2783.
van den Wijngaard A.J., van der Kamp K.W., van der Ploeg J., Pries F., Kazemier B., Janssen D.B. Degradation of 1,2-dichloroethane by Ancylobacter aquaticus and other facultative methylotrophs // Appl. Environ. Microbiol. 1992. V. 58. P. 976–983.
Varghese N.J., Mukherjee S., Ivanova N., Konstantinidis K.T., Mavrommatis K., Kyrpides N.C., Pati A. Microbial species delineation using whole genome sequences // Nucl. Acids Res. 2015. V. 43. P. 6761–6771.
Xin Y.H., Zhou Y.G., Chen W.X. Ancylobacter polymorphus sp. nov. and Ancylobacter vacuolatus sp. nov. // Int. J. Syst. Evol. Microbiol. 2006. V. 56. P. 1185–1188.
Xin Y.H., Zhou Y.G., Zhou H.L., Chen W.X. Ancylobacter rudongensis sp. nov., isolated from roots of Spartina anglica // Int. J. Syst. Evol. Microbiol. 2004. V. 54. P. 385–388.
Wang P., Sheng H., Hong Yi, Debnath S.Ch., Cen Yan, Li K., Chen G., Xu J., Wu F., Guo Zh., Zheng D. Ancylobacter gelatini sp. nov., isolated from beach sediment of Zhairuo Island, China // Arch. Microbiol. 2022. V. 204. Art. 430.