Abstract
A novel Gram-negative, rod-shaped, aerobic, oxidase-positive and catalase-negative bacterium, designated strain SM1970T, was isolated from a seawater sample collected from the Mariana Trench. Strain SM1970T grew at 15-37 oC and with 1–5% (w/v) NaCl. It hydrolyzed colloidal chitin, agar and casein but did not reduce nitrate to nitrite. Phylogenetic analysis based on the 16S rRNA gene sequences revealed that strain SM1970T formed a distinct lineage close to the genus Catenovulum within the family Alteromonadaceae, sharing the highest sequence similarity (93.6%) with type strain of Catenovulum maritimum but < 93.0% sequence similarity with those of other known species in the class Gammaproteobacteria. The major fatty acids of strain SM1970T were summed feature 3 (C16: 1 ω7c and/or C16: 1 ω6c), C16: 0 and summed feature 8 (C18: 1 ω7c and/or C18: 1 ω6c). The major polar lipids of the strain included phosphatidylethanolamine and phosphatidylglycerol and its main respiratory quinone was ubiquinone 8. The draft genome of strain SM1970T consisted of 77 scaffolds and was 4,172,146 bp in length, containing a complete set of genes for chitin degradation. The average amino acid identity (AAI) values between SM1970T and type strains of known Catenovulum species were 56.6–57.1% while the percentage of conserved proteins (POCP) values between them were 28.5–31.5%. The genomic DNA G + C content of strain SM1970T was 40.1 mol%. On the basis of the polyphasic analysis, strain SM1970T is considered to represent a novel species in a novel genus of the family Alteromonadaceae, for which the name Marinifaba aquimaris is proposed with the type strain being SM1970T (= MCCC 1K04323T = KCTC 72844T).
Similar content being viewed by others
Data availability
All data generated or analysed during this study are included in this published article (and its supplementary information files).
References
Aziz RK, Bartels D, Best AA, DeJongh M, Disz T, Edwards RA, Formsma K, Gerdes S, Glass EM, Kubal M, Meyer F, Olsen GJ, Olson R, Osterman AL, Overbeek RA, McNeil LK, Paarmann D, Paczian T, Parrello B, Pusch GD, Reich C, Stevens R, Vassieva O, Vonstein V, Wilke A, Zagnitko O (2008) The RAST Server: rapid annotations using subsystems technology. BMC Genom 9:75
Chun J, Lee JH, Jung Y, Kim M, Kim S, Kim BK, Lim YW (2007) EzTaxon: a web-based tool for the identification of prokaryotes based on 16S ribosomal RNA gene sequences. Int J Syst Evol Microbiol 57:2259–2261
Collins MD, Jones D (1980) Lipids in the classification and identification of coryneform bacteria containing peptidoglycans based on 2,4-diaminobutyric acid. J Appl Bacteriol 48:459–470
Felsenstein J (1981) Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol 17:368–376
Felsenstein J (1985) Confidence-limits on phylogenies—an approach using the bootstrap. Evolution 39:783–791
Fitch WM (1971) Toward defining the course of evolution: minimum change for a specific tree topology. Syst Zool 20:406–416
Fotedar R, Caldwell ME, Sankaranarayanan K, Al-Zeyara A, Al-Malki A, Kaul R, Marri MA, Al-Shamari HS, Lawson PA (2020) Ningiella ruwaisensis gen. nov. sp. nov. a member of the family Alteromonadaceae isolated from marine water of the Arabian Gulf. Int J Syst Evol Microbiol 70:4130–4138
Glud RN, Wenzhöfer F, Middelboe M, Oguri K, Turnewitsch R, Canfield DE, Kitazato H (2013) High rates of microbial carbon turnover in sediments in the deepest oceanic trench on Earth. Nat Geosci 6:284–288
Ivanova EP, Mikhailov VV (2001) A new family, Alteromonadaceae fam. nov., including marine proteobacteria of the genera Alteromonas, Pseudoalteromonas, Idiomarina, and Colwellia. Microbiology 70:10–17
Ivanova EP, Zhukova NV, Svetashev VI, Gorshkova NM, Kurilenko VV, Frolova GM, Mikhailov VV (2000) Evaluation of phospholipid and fatty acid compositions as chemotaxonomic markers of Alteromonas-like proteobacteria. Curr Microbiol 41:341–345
Ivanova EP, Flavier S, Christen R (2004) Phylogenetic relationships among marine Alteromonas-like proteobacteria: emended description of the family Alteromonadaceae and proposal of Pseudoalteromonadaceae fam. nov., Colwelliaceae fam nov, Shewanellaceae fam. nov., Montellaceae fam. nov, Ferrimonadaceae fam. nov., Idiomarinaceae fam. nov. and Psychromonadaceae fam. nov. Int J Syst Evol Microbiol 54:1773–1788
Jackman SD, Vandervalk BP, Mohamadi H, Chu J, Yeo S, Hammond SA, Jahesh G, Khan H, Coombe L, Warren RL, Birol I (2017) ABySS 2.0: resource-efficient assembly of large genomes using a Bloom filter. Genome Res 27:768–777
Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide-sequences. J Mol Evol 16:111–120
Komagata K, Suzuki K (1987) 4 Lipid and cell-wall analysis in bacterial systematics. Methods Microbiol 19:161–207
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
Lagesen K, Hallin P, Rødland EA, Stærfeldt HH, Rognes T, Ussery DW (2007) RNAmmer: consistent and rapid annotation of ribosomal RNA genes. Nucleic Acids Res 35:3100–3108
Li DQ, Zhou YX, Liu T, Chen GJ, Du ZJ (2015) Catenovulum maritimus sp. nov., a novel agarolytic gammaproteobacterium isolated from the marine alga Porphyra yezoensis Ueda (AST58-103), and emended description of the genus Catenovulum. Antonie Van Leeuwenhoek 108:427–434
Liu JW, Zheng YF, Lin HY, Wang XC, Li M, Liu Y, Yu M, Zhao MX, Pedentchouk N, Lea-Smith DJ, Todd JD, Magill CR, Zhang WJ, Zhou S, Song DL, Zhong HH, Xin Y, Yu M, Tian JW, Zhang XH (2019) Proliferation of hydrocarbon-degrading microbes at the bottom of the Mariana Trench. Microbiome 7:47
López-Pérez M, Rodriguez-Valera F (2014) The family Alteromonadaceae. The Prokaryotes, pp 69–92
Lowe TM, Eddy SR (1997) tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res 25:955–964
Luo CW, Rodriguez-R LM, Konstantinos KT (2014) MyTaxa: an advanced taxonomic classifier for genomic and metagenomic sequences. Nucleic Acids Res 42:e73
Meier-Kolthoff JP, Auch AF, Klenk HP, Göker M (2013) Genome sequence-based species delimitation with confidence intervals and improved distance functions. BMC Bioinform 14:60
Murray RGE, Doetsch RN, Robinow CF (1994) Determinative and cytological light microscopy. In: Gerhardt P, Murray RGE, Wood WA, Krieg NR (eds) Methods for general and molecular bacteriology. American Society for Microbiology, Washington, DC, pp 21–41
Nunoura T, Takaki Y, Hirai M, Shimamura S, Makabe A, Koide O, Kikuchi T, Miyazaki J, Koba K, Yoshida N, Sunamura M, Takai K (2015) Hadal biosphere: insight into the microbial ecosystem in the deepest ocean on earth. P Natl Acad Sci 112:E1230–E1236
Pérez-Catalua A, Salas-Massó N, Diéguez AL, Balboa S, Lema A, Romalde JL, Figueras MJ (2018) Revisiting the taxonomy of the genus Arcobacter: getting order from the chaos. Front Microbiol 9:2077
Qin QL, Xie BB, Zhang XY, Chen XL, Zhou BC, Zhou JZ, Oren A, Zhang YZ (2014) A proposed genus boundary for the prokaryotes based on genomic insights. J Bacteriol 196:2210–2215
Rodriguez -RLM, Konstantinidis KT (2014) Bypassing cultivation to identify bacterial species. Microbe 9:111–118
Rzhetsky A, Nei M (1992) A simple method for estimating and testing minimum-evolution trees. Mol Biol Evol 9:945–967
Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425
Sasser M (1990) Identification of bacteria by gas chromatography of cellular fatty acids. USFCC Newsl 20:1–6
Shi MJ, Du WJ, Wang C, Chen GJ, Du ZJ (2017) Catenovulum sediminis sp nov., isolated from coastal sediment. Int J Syst Evol Microbiol 67:3894–3898
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 607–654
Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680
Wang YJ, Jiang WX, Zhang YS, Cao HY, Zhang Y, Chen XL, Li CY, Wang P, Zhang YZ, SongXY, Li PY (2019) Structural insight into chitin degradation and thermostability of a novel endochitinase from the glycoside hydrolase family 18. Front Microbiol 10:2457
Won-Jae C, Park JS, Kwak MJ, Kim JF, Chang YK, Hong SK (2013) Isolation and characterization of a novel agar-degrading marine bacterium, Gayadomonas joobiniege gen, nov, sp nov., from the Southern Sea, Korea. J Microbiol Biotech 23:1509–1518
Yan SL, Yu M, Wang Y, Shen C, Zhang XH (2011) Catenovulum agarivorans gen. nov., sp nov., a peritrichously flagellated, chain-forming, agar-hydrolysing gammaproteobacterium from seawater. Int J Syst Evol Microbiol 61:2866–2873
Yoon SH, Ha SM, Kwon S, Lim J, KimY, Seo H, Chun J (2017a) Introducing EzBioCloud: a taxonomically united database of 16S rRNA gene sequences and whole-genome assemblies. Int J Syst Evol Microbiol 67:1613–1617
Yoon SH, Ha SM, Lim J, Kwon S, Chun J (2017b) A large-scale evaluation of algorithms to calculate average nucleotide identity. Antonie Van Leeuwenhoek 110:1281–1286
Zhao XX, Liu JW, Zhou S, Zheng YF, Wu YH, Kogure K, Zhang XH (2020) Diversity of culturable heterotrophic bacteria from the Mariana Trench and their ability to degrade macromolecules. Marine Life Sci Technol 2:181–193
Acknowledgements
We sincerely thank Jing-Yao Qu, Jing Zhu and Zhi-Feng Li from State Key Laboratory of Microbial Technology of Shandong University for help and guidance in LC-MS and professor Aharon Oren from the Hebrew University of Jerusalem for his assistance in naming the new genus.
Funding
This work was supported by the National Key Research and Development Program of China (grants 2018YFC0310704 and 2018YFC1406504, awarded to Xiu-Lan Chen and Xiao-Yan Song), the National Science Foundation of China (grants 31971535, U1706207, 42076151, 31900023, 42076229 and 31870101, awarded to Xiao-Yan Song, Yu-zhong Zhang, Xi-ying Zhang, Hai-Nan Su, Chun-Yang Li and Qi-Long Qin, respectively), Major Scientific and Technological Innovation Project (MSTIP) of Shandong Province (2019JZZY010817 awarded to Yu-Zhong Zhang), Taishan Scholars Program of Shandong Province (tspd20181203 awarded to Yu-Zhong Zhang). Persons employed by the funders had no role in the study or in the preparation of the article or decision to publish.
Author information
Authors and Affiliations
Contributions
Xi-ying Zhang, Yu-zhong Zhang, Xiu-lan Chen designed and coordinated this study; Xin Sui performed experiments and drafted the manuscript; Xiao-yan He, Ning-hua Liu and Mei-ling Sun helped in experiments and interpreting the results; Yan-ru Dang, Qian-qian Cha, Qi-long Qin, Hui-hui Fu and Hai-nan Su collected the samples and helped in experiments; Chun-yang Li, Xiao-yan Song, Xiu-lan Chen, Yu-zhong Zhang, Xi-ying Zhang and Xiao-yan He revised the manuscript.
Corresponding authors
Ethics declarations
Conflict of interest
The authors have declared that no conflict of interest exists.
Ethical approval
This article does not contain any studies with human participants or animals performed by any of the authors.
Informed consent
All authors agree to publish.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Xin Sui and Xiao-yan He have contributed equally to this work.
Supplementary information
Rights and permissions
About this article
Cite this article
Sui, X., He, Xy., Liu, Nh. et al. Marinifaba aquimaris gen. nov., sp. nov., a novel chitin‐degrading gammaproteobacterium in the family Alteromonadaceae isolated from seawater of the Mariana Trench. Antonie van Leeuwenhoek 114, 947–955 (2021). https://doi.org/10.1007/s10482-021-01568-w
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10482-021-01568-w