Skip to main content
SpringerLink
Log in

Cysteiniphilum marinum sp. nov., isolated from coastal seawater

  • Original Paper
  • Published:
Antonie van Leeuwenhoek Aims and scope Submit manuscript

Abstract

Six aerobic Gram-negative bacteria were isolated from seawater in Guangdong Province, P.R. China. Cells were observed to be Gram-negative, aerobic, non-motile and non-spore forming. Growth of the designated type strain 19X3-30T occurred at a temperature range of 14–37 °C (optimum, 28 °C), a pH range of 6.0–8.0 (optimum, pH 7) and up to 7.5% NaCl (optimum, 1.5%; w/v), and was enhanced by CO2 and L-cysteine supplementation. The major polar lipids identified in strain 19X3-30T were diphosphatidylglycerol, phosphatidylethanolamine and phosphatidylglycerol. The principal cellular fatty acids profile showed the presence of anteiso-C15:0, anteiso-C17:0 and C18:0 (> 8% of total fatty acids), and the respiratory quinone was ubiquinone 8 (UQ-8). According to the analysis of 16S rRNA gene sequences, these strains represented a novel species within the family Fastidiosibacteraceae, sharing maximum similarities with Cysteiniphilum litorale DSM 101832T (96.6%) and Cysteiniphilum halobium DSM 103992T (95.3%). Phylogenetic dendrograms based on 16S rRNA gene and protein marker genes from the genomic sequences both indicated that the strains formed a monophyletic lineage closely linked to the genus Cysteiniphilum, which was also supported by the UPGMA dendrogram based on the MALDI-TOF MS profile. The genomic DNA G + C contents of six strains ranged from 38.0% to 38.1%. Based on different taxonomic genomic metrics, phylogeny and phenotypic features, we propose that the strains warrant the assignment to a novel species, for which the name Cysteiniphilum marinum sp. nov. is proposed. The type strain is 19X3-30T (= KCTC 82154T = CGMCC 1.18585T).

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

Abbreviations

AAI:

Average amino acid identity

ANI:

Average nucleotide identity

BCYEα :

Buffered charcoal yeast extract medium supplemented with α-ketoglutaric acid

CLSI:

The Clinical and Laboratory Standards Institute

FAME:

Fatty acid methyl ester

GC:

Gas chromatography

G + C:

Guanine-plus-cytosine

HPLC:

High performance liquid chromatography

MALDI-TOF MS:

Matrix-Assisted Laser Desorption Ionization Time of Flight Mass Spectrometry

MEGA:

Molecular Evolutionary Genetics Analysis

References

  • Abbas MM, Malluhi QM, Balakrishnan P (2014) Assessment of de novo assemblers for draft genomes: a case study with fungal genomes. BMC Genomics 15:S10

    Article  PubMed  PubMed Central  Google Scholar 

  • Aslanzadeh J (2006) Biochemical profile-based microbial identification systems. In: Tang YW, Stratton CW (eds) Advanced techniques in diagnostic microbiology. Springer, New York, pp 87–121

    Google Scholar 

  • Brevik OJ, Ottem KF, Kamaishi T, Watanabe K, Nylund A (2011) Francisella halioticida sp. nov., a pathogen of farmed giant abalone (Haliotis gigantea) in Japan. J Appl Microbiol 111:1044–1056

    Article  CAS  PubMed  Google Scholar 

  • Chun J, Oren A, Ventosa A, Christensen H, Arahal DR, Costa MS, Rooney AP, Yi H, Xu XW, Meyer S, Trujillo M (2018) Proposed minimal standards for the use of genome data for the taxonomy of prokaryotes. Int J Syst Evol Microbiol 68:461–466

    Article  CAS  PubMed  Google Scholar 

  • Clinical and Laboratory Standards Institute (2015) Methods for antimicrobial dilutioon and disk susceptibility testing of infre quently isolated or fasidious bacteria; approved guideline 2nd ed. Wayne, PA, CLSI document M45-A3

  • Collins MD, Jones D (1980) Lipids in the classification and identification of coryneform bacteria containing peptidoglycan based on 2,4-diaminobutyric acid. J Appl Bacteriol 48:459–470

    Article  CAS  Google Scholar 

  • Collins MD, Pirouz T, Goodfellow M, Minnikin DE (1977) Distribution of menaquinones in actinomycetes and corynebacteria. J Gen Microbiol 100:221–230

    Article  CAS  PubMed  Google Scholar 

  • Dennis DT, Inglesby TV, Henderson DA, Bartlett JG, Ascher MS, Eitzen E, Fine AD, Friedlander AM, Hauer J, Layton M, Lillibridge SR, McDade JE, Osterholm MT, O’Toole T, Parker G, Perl TM, Russell PK, Tonat K, Working Group on Civilian Biodefense (2001) Tularemia as a biological weapon: medical and public health management. JAMA 285:2763–2773

  • Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ellingsen T, Inami M, Gjessing MC, Van Nieuwenhove K, Larsen R, Seppola M, Lund V, Schrøder MB (2011) Francisella noatunensis in Atlantic cod (Gadus morhua L.); waterborne transmission and immune responses. Fish Shellfish Immunol 31:326–333

    Article  CAS  PubMed  Google Scholar 

  • Felsenstein J (1981) Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol 17:368–376

    Article  CAS  PubMed  Google Scholar 

  • Felsenstein J (1985) Confidence limit on phylogenies: an approach using the bootstrap. Evolution 39:783–791

    Article  PubMed  Google Scholar 

  • Fitch WM (1971) Toward defining the course of evolution: minimum change for a specific tree topology. Syst Biol 20:406–416

    Article  Google Scholar 

  • Frank JA, Reich CI, Sharma S, Weisbaum JS, Wilson BA, Olsen GJ (2008) Critical evaluation of two primers commonly used for amplification of bacterial 16S rRNA genes. Appl Environ Microbiol 74:2461–2470

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Giovannoni SJ (1991) The polymerase chain reaction. In: Stackebrandt E, Goodfellow M (eds) Modern microbiological methods: nucleic acids techniques in bacterial systematics. Wiley, New York, pp 177–203

    Google Scholar 

  • Kim M, Oh HS, Park SC, Chun J (2014) Towards a taxonomic coherence between average nucleotide identity and 16S rRNA gene sequence similarity for species demarcation of prokaryotes. Int J Syst Evol Microbiol 64:346–351

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Kroppenstedt RM (1982) Separation of bacterial menaquinones by HPLC using reverse phase (RP18) and a silver loaded ion exchanger as stationary phases. J Liq Chromatogr 5:2359–2367

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Letunic I, Bork P (2016) Interactive tree of life (iTOL) v3: an online tool for the display and annotation of phylogenetic and other trees. Nucleic Acids Res 44:W242–W245

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu L, Salam N, Jiao JY, Shun-Mei E, Chen C, Fang BZ, Qu PH (2017) Cysteiniphilum litorale gen. nov., sp. nov., isolated from coastal seawater. Int J Syst Evol Microbiol 67:2178–2183

    Article  CAS  PubMed  Google Scholar 

  • Logan NA, Vos PD (2009) The genus Bacillus. In: Vos PD, Garrity GM, Jones D, Krieg ND, Ludwig W, Rainey FA, Schleifer KH, Whitman WB (eds) Bergey’s Manual of Systematic Bacteriology. Springer, New York

    Google Scholar 

  • Ming H, Yin YR, Li S, Nie GX, Yu TT, Zhou EM, Liu L, Dong L, Li WJ (2014) Thermus caliditerrae sp. nov., a novel thermophilic species isolated from a geothermal area. Int J Syst Evol Microbiol 64:650–656

    Article  CAS  PubMed  Google Scholar 

  • Minnikin DE, Collins MD, Goodfellow M (1979) Fatty acid and polar lipid composition in the classification of Cellulomonas, Oerskovia and related taxa. J Appl Bacteriol 47:87–95

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Relich RF, Humphries RM, Mattison HR, Miles JE, Simpson ER, Corbett IJ, Schmitt BH, May M (2015) Francisella philomiragia bacteremia in a patient with acute respiratory insufficiency and acute-on-chronic kidney disease. J Clin Microbiol 53:3947–3950

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Richter M, Rosselló-Móra R, Oliver Glöckner F, Peplies J (2015) JSpeciesWS: a web server for prokaryotic species circumscription based on pairwise genome comparison. Bioinformatics 32:929–931

    Article  PubMed  PubMed Central  Google Scholar 

  • Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425

    CAS  PubMed  Google Scholar 

  • Seibold E, Maier T, Kostrzewa M, Zeman E, Splettstoesser W (2010) Identification of Francisella tularensis by whole-cell matrix-assisted laser desorption ionization-time of flight mass spectrometry: fast, reliable, robust, and cost-effective differentiation on species and subspecies levels. J Clin Microbiol 48:1061–1069

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Smibert RM, Krieg NR (1994) Phenotypic characterization. In: Gerhardt P, Murray RGE, Wood WA et al (eds) Methods for general and molecular bacteriology. American Society for Microbiology, Washington, pp 607–654

    Google Scholar 

  • Stamatakis A (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30:1312–1313

    Article  PubMed  PubMed Central  Google Scholar 

  • Staples JE, Kubota KA, Chalcraft LG, Mead PS, Petersen JM (2006) Epidemiologic and molecular analysis of human tularemia, United States, 1964–2004. Emerg Infect Dis 12:1113–1118

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sun C, Wang RJ, Su Y, Fu GY, Zhao Z, Yu XY, Zhang CY, Chen C, Han SB, Huang MM, Lv ZB, Wu M (2017) Hyphobacterium vulgare gen. nov., sp. nov., a novel alphaproteobacterium isolated from seawater. Int J Syst Evol Microbiol 67:1169–1176

    Article  CAS  PubMed  Google Scholar 

  • Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The clustal_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thompson CC, Chimetto L, Edwards RA, Swings J, Stackebrandt E, Thompson FL (2013) Microbial genomic taxonomy. BMC Genomics 14:913

    Article  PubMed  PubMed Central  Google Scholar 

  • Wu M, Scott AJ (2012) Phylogenomic analysis of bacterial and archaeal sequences with AMPHORA2. Bioinformatics 28:1033–1034

    Article  CAS  PubMed  Google Scholar 

  • Xiao M, Salam N, Liu L, Jiao JY, Zheng ML, Wang J, Li S, Chen C, Li WJ, Qu PH (2018) Fastidiosibacter lacustris gen. nov., sp. nov., isolated from a lake water sample, and proposal of Fastidiosibacteraceae fam. nov. within the order Thiotrichales. Int J Syst Evol Microbiol 68:347–352

    Article  CAS  PubMed  Google Scholar 

  • Xiao M, Zheng ML, Salam N, Jiao JY, Dong L, Liu L, Chen C, Li WJ, Qu PH (2019) Facilibium subflavum gen. nov., sp. nov. and Cysteiniphilum halobium sp. nov., new members of the family Fastidiosibacteraceae isolated from coastal seawater. Int J Syst Evol Microbiol 69:3757–3764

    Article  CAS  PubMed  Google Scholar 

  • Xu P, Li WJ, Tang SK, Zhang YQ, Chen GZ, Chen HH, Xu LH, Jiang CL (2005) Naxibacter alkalitolerans gen. nov., sp. nov., a novel member of the family ‘Oxalobacteraceae’ isolated from China. Int J Syst Evol Microbiol 55:1149–1153

    Article  CAS  PubMed  Google Scholar 

  • Yoon SH, Ha SM, Kwon S, Lim J, Kim Y, Seo H, Chun J (2017) Introducing EzBioCloud: a taxonomically united database of 16S rRNA gene sequences and whole-genome assemblies. Int J Syst Evol Microbiol 67:1613–1617

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhou H, Yang Q, Shen L, Yao Y, Xu J, Ye J, Wu X, Yu Y, Li Z, Zhou J, Yang S (2020) Seawater-associated highly pathogenic Francisella hispaniensis infections causing multiple organ failure. Emerg Infect Dis 26:2424–2428

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

This research was supported by funds received from the Natural Science Foundation of Guangdong Province (2020A1515011119), Guangdong Province Ordinary Universities Characteristic Innovation Project (2018KTSCX042), and the Science and Technology Planning Project of Guangdong Province (2017A020215068).

Author information

Author notes

  1. Hai-Min Luo and Jun-Hui Feng have contributed equally to this work.

Authors and Affiliations

  1. The Second Clinical College, Guangzhou University of Chinese Medicine, Guangzhou, 510120, People’s Republic of China

    Hai-Min Luo, Jun-Hui Feng & Liang-Hui Li

  2. Department of Clinical Laboratory, Guangdong Provincial Hospital of Traditional Chinese Medicine, Guangzhou, 510006, People’s Republic of China

    Fu Chen & Ping-Hua Qu

  3. School of Nursing, Guangdong Pharmaceutical University, Guangzhou, 510006, People’s Republic of China

    Ru-Qin Liu

  4. Department of Dermatology, Guangdong Provincial Hospital of Traditional Chinese Medicine, Guangzhou, 510006, People’s Republic of China

    Ying Lin

  5. State Key Laboratory of Biocontrol, Guangdong Provincial Key Laboratory of Plant Resources and Southern Marine Science and Engineering Guangdong Laboratory (Zhuhai), School of Life Sciences, Sun Yat-Sen University, Guangzhou, 510275, People’s Republic of China

    Meng-Meng Li, Wen-Jun Li & Min Xiao

Authors
  1. Hai-Min Luo
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jun-Hui Feng
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Liang-Hui Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Meng-Meng Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Ru-Qin Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Fu Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Ying Lin
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Wen-Jun Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Ping-Hua Qu
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Min Xiao
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

WJL, PHQ and MX designed research and project outline. HML, JHF, RQL, MML and YL performed the experiments. JHF, LHL MML and FC analysed the data. HML and JHF drafted the manuscript. All authors have read and approved the final manuscript.

Corresponding authors

Correspondence to Ping-Hua Qu or Min Xiao.

Ethics declarations

Conflict of interest

All the authors have declared that there are no conflicts of interest.

Additional information

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.

Supplementary file1 (DOCX 18475 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Luo, HM., Feng, JH., Li, LH. et al. Cysteiniphilum marinum sp. nov., isolated from coastal seawater. Antonie van Leeuwenhoek 114, 1079–1089 (2021). https://doi.org/10.1007/s10482-021-01579-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10482-021-01579-7

Keywords

Search

Navigation