Abstract
A Gram-stain-negative, rod-shaped, glide, non-flagellated, and facultatively anaerobic bacterial strain, designated as Z654T, was isolated from the gut of abalone Haliotis discus hannai from Rongcheng, Shandong province, China. Cells are 0.2–0.8 μm in width and 0.7–3.4 μm in length. Cells grew best at 30 °C (range, 15–37 °C), pH 7.0 (range, 6.0–8.5) and NaCl concentration of 2.0% (w/v) (range, 1–10%). According to the phylogenetic analysis of 16S rRNA gene sequence, the strain belongs to the genus Halocynthiibacter and the closest strain is Halocynthiibacter arcticus KCTC 42129 T (97.12%). The genome size of strain Z654T was 3,296,250 bp and the DNA G + C content was 54.2 mol%. The average nucleotide identity (ANI) scores and digital DNA–DNA hybridization (dDDH) scores with H. arcticus KCTC 42129 T were 70% and 14.6–18.2%, respectively. The predominant quinone was Q-10 and the major fatty acids were C18:0, C18:1 ω7c 11-methyl and summed feature 8. The polar lipids consisted of phosphatidylcholine, phosphatidylglycerol, unidentified aminolipid and unidentifed lipids. Based on the phenotypic, phylogenetic and chemotaxonomic data, strain Z654T was considered to represent a novel species of the genus Halocynthiibacter, for which the name Halocynthiibacte halioticoli sp. nov., is proposed. The type strain is Z654T (= MCCC 1H00503T = KCTC 92003 T).
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
The data that support the finding of this study are openly avaiable in reference.
Abbreviations
- dDDH:
-
Digital DNA–DNA hybridization
- GGDC:
-
Genome-to-genome distance calculator
- ANI:
-
Average nucleotide identity
- APL:
-
Aminophospholipid
- PC:
-
Phosphatidylcholine
- PG:
-
Phosphatidylglycerol
References
Baek K, Lee YM, Shin SC, Hwang K, Hwang CY, Hong SG, Lee HK (2015) Halocynthiibacter arcticus sp. nov., isolated from Arctic marine sediment. Int J Syst Evol Microbiol. https://doi.org/10.1099/ijsem.0.000507
Bowman JP (2000) Description of Cellulophaga algicola sp. nov., isolated from the surfaces of Antarctic algae, and reclassification of Cytophaga uliginosa (ZoBell and Upham 1944) Reichenbach 1989 as Cellulophaga uliginosa comb. nov. Int J Syst Evol Microbiol 50:1861–1868. https://doi.org/10.1099/00207713-50-5-1861
Campeão ME, Swings J, Silva BS, Otsuki K, Thompson FL, Thompson CC (2019) “Candidatus Colwellia aromaticivorans” sp. nov., “Candidatus Halocyntiibacter alkanivorans” sp. nov., and “Candidatus Ulvibacter alkanivorans” sp. nov. Genome Sequences. Microbiol Resour Announc. https://doi.org/10.1128/MRA.00086-19
Chaudhari NM, Gupta VK, Dutta C (2016) BPGA- an ultra-fast pan-genome analysis pipeline. Sci Rep 13(6):24373. https://doi.org/10.1038/srep24373
Chiriac C, Baricz A, Coman C (2018) Draft Genome Sequence of Janthinobacterium sp. Strain ROICE36, a Putative Secondary Metabolite-Synthesizing Bacterium Isolated from Antarctic Snow. Genome Announc. https://doi.org/10.1128/genomeA.01553-17
Chun J, Oren A, Ventosa A, Christensen H, Arahal DR, da Costa MS, Rooney AP, Yi H, Xu XW, De Meyer S, Trujillo ME (2018) Proposed minimal standards for the use of genome data for the taxonomy of prokaryotes. Int J Syst Evol Microbiol 68(1):461–466. https://doi.org/10.1099/ijsem.0.002516
Collins MD (1994) Isoprenoid quinones. In: Goodfellow M, O’Donnell AG (eds) Chemical methods in prokaryotic systematics. Wiley, Chichester, pp 345–401
Cowan ST, Steel KJ (1974) Bacterial characters and characterization, 2nd edn. Cambridge University Press, Cambridge
Cui Y, Wang M, Zheng Y, Miao K, Qu X (2021) The Carbohydrate Metabolism of Lactiplantibacillus plantarum. Int J Mol Sci 22(24):13452. https://doi.org/10.3390/ijms222413452
Dong XZ, Cai MY. Determination of biochemical characteristics. Manual for the Systematic Identification of General Bacteria, 398. Beijing: Science Press; 2001. p. 370
Du ZJ, Wang Y, Dunlap C, Rooney AP, Chen G- J, (2014) Draconibacterium orientale gen. nov., sp. nov., isolated from two distinct marine environments, and proposal of Draconibacteriaceae fam. nov. Int J Syst Evol Microbiol 64:1690–1696. https://doi.org/10.1099/ijs.0.056812-0
Gao X, Zhou F, Chen CTA (2014) Pollution status of the Bohai Sea: an overview of the environmental quality assessment related trace metals. Environ Int 62:12–30. https://doi.org/10.1016/j.envint.2013.09.019
Jiang H, Tang S, Qin D, Chen Z, Wang J, Bai S, Mou Z (2015) Heavy metals in sea cucumber juveniles from coastal areas of Bohai and Yellow seas, north China. Bull Environ Contam Toxicol 94(5):577–582. https://doi.org/10.1007/s00128-014-1432-1
Kamekura M (1993) Lipids of extreme halophiles. In: Vreeland RH, Hochstein LI (eds) The Biology of Halophilic Bacteria. CRC Press, Boca Raton, pp 135–161
Kim YO, Park S, Kim H, Park DS, Nam BH, Kim DG, Yoon JH (2014) Halocynthiibacter namhaensis gen nov., sp. nov., a novel alphaproteobacterium isolated from sea squirt Halocynthia roretzi. Antonie Van Leeuwenhoek. https://doi.org/10.1007/s10482-014-0142-3
Kroppenstedt RM (1982) Separation of bacterial menaquinones by HPLC using reverse phase (RP18) and a silver loaded ion exchanger as stationary phases. J Liq Chrom 5:2359–2367. https://doi.org/10.1080/01483918208067640
Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: Molecular Evolutionary Genetics Analysis across computing platforms. MOL BIOL EVOL 35:1547–1549. https://doi.org/10.1093/molbev/msy096
Kuykendall LD, Roy MA, Oneill JJ, Devine TE (1988) Fattyacids, antibiotic-resistance, and deoxyribonucleic-acid homology groups of Bradyrhizobium-japonicum. Int J Syst Bacteriol 38:358–361. https://doi.org/10.1099/00207713-38-4-358
Liu QQ, Wang Y, Li J, Du ZJ, Chen GJ (2014) Saccharicrinis carchari sp. nov., isolated from a shark, and emended descriptions of the genus Saccharicrinis and Saccharicrinis fermentans. Int J Syst Evol Microbiol 64:2204–2209. https://doi.org/10.1099/ijs.0.061986-0
Luo W, Lu Y, Wang T, Hu W, Jiao W, Naile JE, Giesy JP (2010) Ecological risk assessment of arsenic and metals in sediments of coastal areas of northern Bohai and Yellow Seas. China Ambio 39(5–6):367–375. https://doi.org/10.1007/s13280-010-0077-5
Nam BH, Jang J, Caetano-Anolles K, Kim YO, Park JY, Sohn H, Yoon SH, Kim H, Kwak W (2018) Microbial community and functions associated with digestion of algal polysaccharides in the visceral tract of Haliotis discus hannai: Insights from metagenome and metatranscriptome analysis. PLoS ONE 13(10):e0205594. https://doi.org/10.1371/journal.pone.0205594
Ojima T, Rahman MM, Kumagai Y, Nishiyama R, Narsico J, Inoue A (2018) Polysaccharide-Degrading Enzymes From Marine Gastropods. Methods Enzymol 605:457–497. https://doi.org/10.1016/bs.mie.2018.01.032
Páez-Espino AD, Nikel PI, Chavarría M, de Lorenzo V (2020) ArsH protects Pseudomonas putida from oxidative damage caused by exposure to arsenic. Environ Microbiol 22(6):2230–2242. https://doi.org/10.1111/1462-2920.14991
Price MN, Dehal PS, Arkin AP (2009) FastTree: computing large minimum evolution trees with profiles instead of a distance matrix. Mol Biol Evol 26(7):1641–1650. https://doi.org/10.1093/molbev/msp077
Qin QL, Xie BB, Zhang XY, Chen XL, Zhou BC, Zhou J, Oren A, Zhang YZ (2014) A proposed genus boundary for the prokaryotes based on genomic insights. J Bacteriol 196(12):2210–2215. https://doi.org/10.1128/JB.01688-14
Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4(4):406–425. https://doi.org/10.1093/oxfordjournals.molbev.a040454
Sato K, Naya M, Hatano Y, Kondo Y, Sato M, Narita Y, Nagano K, Naito M, Nakayama K, Sato C (2021) Colony Spreading of the Gliding Bacterium Flavobacterium Johnsoniae in the Absence of the Motility Adhesin. SprB Sci Rep 11(1):967. https://doi.org/10.1038/s41598-020-79762-5
Smibert RM, Krieg NR (1994) Phenotypic characterization. In: Methods for general and molecular bacteriology. American Society For Microbiology, pp 611–651. https://doi.org/10.1002/food.19960400226
Tindall BJ (1990) Lipid composition of Halobacterium lacusprofundi. FEMS Microbiol Lett 66:199–202
Trifinopoulos J, Nguyen L-T, von Haeseler A, Minh BQ (2016) W-IQ-TREE: a fast online phylogenetic tool for maximum likelihood analysis. Nucleic Acids Res 44:W232–W235. https://doi.org/10.1093/nar/gkw256
Wysocki R, Bobrowicz P, Ułaszewski S (1997) The Saccharomyces cerevisiae ACR3 gene encodes a putative membrane protein involved in arsenite transport. J Biol Chem. https://doi.org/10.1074/jbc.272.48.30061
Xing J, Chia FS (1997) Heavy metal accumulation in tissue/organs of a sea cucumber, Holothuria leucospilota. In: Asia-Pacific conference on science and management of coastal environment pp 17–23. https://doi.org/10.1023/A:1003028601518
Yang Z (2007) PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol 24(8):1586–1591. https://doi.org/10.1093/molbev/msm088
Yoon SH, Ha SM, Lim J, Kwon S, Chun J (2017) A large-scale evaluation of algorithms to calculate average nucleotide identity. Antonie Van Leeuwenhoek 110(10):1281–1286. https://doi.org/10.1007/s10482-017-0844-4
Zhang H, Yohe T, Huang L, Entwistle S, Wu P, Yang Z, Busk PK, Xu Y, Yin Y (2018) dbCAN2: a meta server for automated carbohydrate-active enzyme annotation. Nucleic Acids Res 46(W1):W95–W101. https://doi.org/10.1093/nar/gky418
Acknowledgements
The implementation of scanning electron microscopy was supported by the Physical–Chemical Materials Analytical and Testing Center of Shandong University at Weihai.
Funding
This work was supported by Science & Technology Fundamental Resources Investigation Program (Grant No. 2022FY101100, 2019FY100700) and the National Natural Science Foundation of China (32070002).
Author information
Authors and Affiliations
Contributions
Meng-Di Zhang wrote the original draft, Yu-Yan Yue wrote the main manuscript text, Dan-Dan Zhang and Yu-Yan Yue completed the total experiment, data curation and formal analysis. Dan-Dan Zhang prepared figure1-2, and Yu-Yan Yue Finish the following chart and table production. All authors reviewed the manuscript.
Corresponding author
Ethics declarations
Conflicts of interests
The authors declare that they have conflict of interest.
Human and animal rights
This article does not contain any studies with animals performed by any of the authors.
Informed consent
Informed consent was obtained from all individual participants included in the study.
Additional information
Communicated by Yusuf Akhter.
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
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Zhang, DD., Yue, YY., Zhang, MD. et al. Halocynthiibacter halioticoli sp. nov., isolated from the viscera of abalone Haliotis discus hannai. Arch Microbiol 205, 350 (2023). https://doi.org/10.1007/s00203-023-03686-7
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00203-023-03686-7