Abstract
A novel aerobic bacterium, strain PS-22 of the genus Moraxella, was isolated from the skin of freshwater pufferfish (Tetraodon cutcutia). Cells were Gram stain negative, aerobic, non-motile, and coccoid. Optimum growth occurred at 28–30 °C and pH 6.5–7.5. The major cellular fatty acids were C18:1 ω9c, C10:0, C16:0, and C12:0 anteiso. The predominant polar lipids were diphosphatidylglycerol, phosphatidylglycerol, phosphatidylethanolamine, phospholipid, amino lipid, and seven unknown lipids. The genome size is 2.68 Mbp, and the DNA G + C content was 43.3%. A gene ontology study revealed that the major fraction of genes were associated with biological processes (46.81%), followed by molecular function (34.27%) and cellular components (18.8%). Comparisons of 16S rRNA gene sequences revealed 99.11–90% sequence similarity with the closely related type strains of the genus Moraxella. The average nucleotide identity (ANI) and average amino acid identity (AAI) of strain PS-22 with reference type strains of the genus Moraxella were below 95–96%, and the corresponding in silico DNA–DNA hybridization (DDH) values were below 70%. A phylogenetic tree based on genome-wide core genes and 16S rRNA gene sequences revealed that strain PS-22 clustered with Moraxella osloensis CCUG350T in both the phylogenetic trees. Genotypic and phenotypic characteristics of strain PS-22 represent a novel species for which Moraxella tetraodonis sp. nov. is proposed. The type strain is PS-22T (= TBRC 15232T = NBRC 115236T).
Similar content being viewed by others
References
Badhai J, Kumari P, Krishnan P, Ramamurthy T, Das SK (2013) Presence of SXT integrating conjugative element in marine bacteria isolated from the mucus of the coral Fungia echinata from Andaman Sea. FEMS Microbiol Lett 338:118–123. https://doi.org/10.1111/1574-6968.12033
Berner R, Schumacher RF, Brandis M, Forster J (1996) Colonization and infection with Moraxella catarrhalis in childhood. Eur J Clin Microbiol Infect Dis 15:506–509. https://doi.org/10.1007/BF01691320
Berrocal AM, Scott MIU, Miller D, Flynn HW (2001) Endophthalmitis caused by Moraxella species. Am J Ophthalmol 132:788–790. https://doi.org/10.1016/s0002-9394(01)01098-4
Bligh EG, Dyer WJ (1959) A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37:911–917. https://doi.org/10.1139/o59-099
Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30:2114–2120. https://doi.org/10.1093/bioinformatics/btu170
Das L, Deb S, Arakawa E, Yamasaki S, Das SK (2022) Pufferfish (Tetraodon cutcutia) sampled from a freshwater river serves as an intermediate reservoir of a sucrose nonfermenting variant of Vibrio cholerae PS-4. Microbiology Spectrum 10:e01221-e1321. https://doi.org/10.1128/spectrum.01221-21
Fernández-Garayzábal JF, Miguela-Villoldo P, Vela AI (eds) (2022) Moraxella. In: Bergey’s Manual of Systematics of Archaea and Bacteria. John Wiley and Sons Inc, USA (in association with Bergey's Manual Trust)
Götz S, Garcia-Gomez JM, Terol J, Williams TD, Nagaraj SH, Nueda MJ, Robles M, Talon M, Dopazo J, Conesa A (2008) High-throughput functional annotation and data mining with the Blast2GO suite. Nucleic Acids Res 36:3420–3435. https://doi.org/10.1093/nar/gkn176
Gurevich A, Saveliev V, Vyahhi N, Tesler G (2013) QUAST: quality assessment tool for genome assemblies. Bioinformatics 29:1072–1075. https://doi.org/10.1093/bioinformatics/btt086
Hoquet F, Higgins R, Lessard P, Vrins A, Marcoux M (1985) Comparison of bacterial and fungal flora in the pharynx of normal horses and horses affected with pharyngitis. Can Vet J 26:342–346
Jannes G, Vaneechoutte M, Lannoo M, Gillis M, Vancanneyt M, Vandamme P, Verschraegen G, Heuverswyn HV, Rossau R (1993) Polyphasic taxonomy leading to the proposal of Moraxella canis sp. nov. for Moraxella catarrhalis-like strains. Int J Syst Bacteriol 43:438–449. https://doi.org/10.1099/00207713-43-3-438
Jiang J, Pan Y, Hu S, Zhang X, Hu B, Huang H, Hong S, Meng J, Li C, Wang K (2014) Halomonas songnenensis sp. nov., a moderately halophilic bacterium isolated from saline and alkaline soils. Int J Syst Evol Microbiol 64:1662–1669. https://doi.org/10.1099/ijs.0.056499-0
Jung YT, Oh TK, Yoon JH (2012) Marinomonas hwangdonensis sp. nov., isolated from seawater. Int J Syst Evol Microbiol 62:2062–2067. https://doi.org/10.1099/ijs.0.036582-0
Kodjo A, Dorier A, Lerondelle C, Richard Y (1994) Isolation of a new biovar of Moraxella bovis from healthy caprine nasal swabs. Small Ruminant Res 15:87–95. https://doi.org/10.1016/0921-4488(94)90064-7
Kodjo A, Tonjum T, Richard Y, Bovre K (1995) Moraxella caprae sp. nov., a new member of the classical moraxellae. Int J Syst Bacteriol 45:467–471. https://doi.org/10.1099/00207713-45-3-467
Kodjo A, Richard Y, Tønjum T (1997) Moraxella boevrei sp. nov., a new Moraxella species found in goats. Int J Syst Evol Microbiol 47:115–121. https://doi.org/10.1099/00207713-47-1-115
Konstantinidis KT, Tiedje JM (2005a) Genomic insights that advance the species definition for prokaryotes. Proc Natl Acad Sci USA 102:2567–2572. https://doi.org/10.1073/pnas.0409727102
Konstantinidis KT, Tiedje JM (2005b) Towards a genome-based taxonomy for prokaryotes. J Bacteriol 87:6258–6264. https://doi.org/10.1128/JB.187.18.6258-6264.2005
Kumari P, Poddar A, Das SK (2014) Marinomonas fungiae sp. nov., isolated from the coral Fungia echinata from the Andaman Sea. Int J Syst Evol Microbiol 64:487–494. https://doi.org/10.1099/ijs.0.054809-0
Meier-Kolthoff JP, Auch AF, Klenk HP, Göker M (2013) Genome sequence-based species delimitation with confidence intervals and improved distance functions. BMC Bioinform. http://www.biomedcentral.com/1471-2105/14/60
Na S-I, Kim YO, Yoon S-H, Ha S-M, Baek I, Chun J (2018) UBCG: up-to-date bacterial core gene set and pipeline for phylogenomic tree reconstruction. J Microbiol 56:280–285. https://doi.org/10.1007/s12275-018-8014-6
Overbeek R, Olson R, Pusch GD, Olsen GJ, Davis JJ, Disz T, Edwards RA, Gerdes S, Parrello B, Shukla M, Vonstein V, Wattam AR, Xia F, Stevens R (2014) The SEED and the Rapid Annotation of microbial genomes using Subsystems Technology (RAST). Nucleic Acids Res 42:D206–D214. https://doi.org/10.1093/nar/gkt1226
Parks DH, Imelfort M, Skennerton CT, Hugenholtz P, Tyson GW (2015) CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes. Genome Res 25:1043–1055. https://doi.org/10.1101/gr.186072.114
Rossau R, Van Landschoot A, Gillis M, De Ley J (1991) Taxonomy of Moraxellaceae fam. nov., a new bacterial family to accommodate the genera Moraxella, Acinetobacter, and Psychrobacter and related organisms. Int J Syst Bacteriol 41:310–319. https://doi.org/10.1099/00207713-41-2-310
Salzberg SL, Delcher AL, Kasif S, White O (1998) Microbial gene identification using interpolated Markov models. Nucleic Acids Res 26:544–548. https://doi.org/10.1093/nar/26.2.544
Sambrook J, Russell DW (2001) Molecular cloning: a laboratory manual. 3rd edn. Cold Spring Harbor, New York
Smibert RM, Krieg NR (1994) Phenotypic characterization. In: Gerhardt P, Murray RGE, Wood WA, Krieg NR (eds) Methods for general and molecular bacteriology. American Society for Microbiology, Washington, DC, pp 607–655
Stamatakis A (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30:1312–1313. https://doi.org/10.1093/bioinformatics/btu033
Staneck JL, Roberts GD (1974) Simplified approach to identification of aerobic actinomycetes by thin layer chromatography. Appl Environ Microbiol 28:226–231. https://doi.org/10.1128/am.28.2.226-231.1974
Tatusova T, DiCuccio M, Badretdin A, Chetvernin V, Nawrocki EP, Zaslavsky L, Lomsadze A, Pruitt KD, Borodovsky M, Ostell J (2016) NCBI prokaryotic genome annotation pipeline. Nucleic Acids Res 44:6614–6624. https://doi.org/10.1093/nar/gkw569
Tønjum T, Caugant DA, Bøvre K (1992) Differentiation of Moraxella nonliquefaciens, M. lucunatu, and M. bovis by using multilocus enzyme electrophoresis and hybridization with pilin-specific DNA probes. J Clin Microbiol 30:3099–3107. https://doi.org/10.1128/jcm.30.12.3099-3107.1992
Travicek M, Dravecky T, Balascak J (1994) Isolation of Chlamydia psittuci and Moraxella bovis from infectious keratoconjunctivitis in lambs. Vet Med (prague) 22:491–496
Verduin CM, Hol C, Fleer A, van Dijk H, van Belkum A (2002) Moraxella catharralis: from emerging to established pathogen. Clin Microbiol Rev 15:125–144. https://doi.org/10.1128/CMR.15.1.125-144.2002
Walker BJ, Abeel T, Shea T, Priest M, Abouelliel A, Sakthikumar S, Cuomo CA, Zeng Q, Wortman J, Young SK (2014) Earl AM (2014) Pilon: an integrated tool for comprehensive microbial variant detection and genome assembly improvement. PLoS ONE 9:e112963. https://doi.org/10.1371/journal.pone.0112963
Wick RR, Judd LM, Gorrie CL, Holt KE (2017) Unicycler: Resolving bacterial genome assemblies from short and long sequencing reads. PLoS Comput Biol 13:e1005595. https://doi.org/10.1371/journal.pcbi.1005595
Acknowledgements
The author LD acknowledges the Council of Scientific and Industrial Research (CSIR), New Delhi, Government of India for providing the research fellowship. We acknowledge the Distributed Information Sub-Center (DISC) at Institute of Life Sciences, Bhubaneswar for the computational facility. We are thankful to Professor B. Schink (Universitaet Konstanz, Germany) for etymological advice.
Funding
This work was supported in part by the funding received from Department of Biotechnology, Government of India (D.O.No. BT/PR7661/AAQ/3/629/2013) to SKD.
Author information
Authors and Affiliations
Contributions
SKD: designed the study. LD: conducted the experiment. LD and SKD: analysed the data and wrote the manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Ethical approval
This study was carried out with approval from the Institutional Animal Ethics Committee (Letter No. V-311-MISC/2017-18/ILS/884).
Additional information
Communicated by Erko Stackebrandt.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Das, L., Das, S.K. Moraxella tetraodonis sp. nov., isolated from freshwater pufferfish (Tetraodon cutcutia) skin. Arch Microbiol 204, 389 (2022). https://doi.org/10.1007/s00203-022-03013-6
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00203-022-03013-6