Skip to main content
SpringerLink
Log in

Sulfuriroseicoccus oceanibius gen. nov., sp. nov., a representative of the phylum Verrucomicrobia with a special cytoplasmic membrane

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

Abstract

Here, we describe a novel bacterial strain, designated T37T, which was isolated from the marine sediment of Xiaoshi Island, PR China. Growth of strain T37T occurs at 15–40 °C (optimum 37 °C), pH 6.0–9.0 (optimum 7.5), and in the presence of 0.5–5.5% (w/v) NaCl (optimum 1.5%). Characteristic biochemical traits of the novel strain include MK-9 as the major menaquinone. The major fatty acids identified were iso-C14:0 and C16:1 ω9c (oleic acid). Phosphatidylethanolamine, phosphatidylglycerol, diphosphatidylglycerol, and phosphoglycolipids were the major cellular polar lipids. The G + C content of genomic DNA was 58.4 mol%. Unusual outer membrane features deduced from the analysis of cell morphology point towards the formation of an enlarged periplasmic space putatively used for the digestion of macromolecules. Phylogenetic analyses based on 16S rRNA genes and the genome indicated that strain T37T represents a novel species and genus affiliated with a distinct family level lineage of the verrucomicrobial subdivision 1. Our polyphasic taxonomy approach places the novel strain in a new genus within the current family Verrucomicrobiaceae, order Verrucomicrobiales, class Verrucomicrobiae. Strain T37T (= KCTC 72799 T = MCCC 1H00391T) is the type strain of a novel species, for which the name Sulfuriroseicoccus oceanibius gen. nov., sp. nov. is proposed.

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
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Data availability

The 16S rRNA gene sequence and the complete genome sequence of strain T37T, are deposited in GenBank under accession numbers MN412654 and CP066776.1, respectively. The type strain T37T can be obtained from the Korean Collection for Type Cultures (KCTC 72799 T) and the Marine Culture Collection of China (MCCC 1H00391T).

Abbreviations

PR:

People’s republic

KCTC:

Korean collection for type cultures

DSMZ:

Leibniz institute german collection of microorganisms and cell cultures

MCCC:

Marine culture collection of china

NBRC:

NITE biological resource center

BD:

Becton dickinson

MEGA:

Molecular evolutionary genetics analysis

MA:

Marine agar 2216

MB:

Marine broth 2216

OD:

Optical density

HPLC:

High-performance liquid chromatography

TLC:

Thin-layer chromatography

References

  • Addinall SG, Holland B (2002) The tubulin ancester, FtsZ, draughtsman, designer and driving force for bacterial cytokinesis. J Mol Biol 318:219–236

    Article  CAS  PubMed  Google Scholar 

  • Albrecht W, Fischer A, Smida J, Stackebrandt E (1987) Verrucomicrobium spinosum, a eubacterium representing an ancient line of descent. Syst Appl Microbiol 10:57–62

    Article  CAS  Google Scholar 

  • Alcock BP, Raphenya AR, Lau T, Kara KT, Mégane B et al (2019) CARD 2020: antibiotic resistome surveillance with the comprehensive antibiotic resistance database. Nucleic Acids Res 48:D517–D525

    PubMed Central  Google Scholar 

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

  • Amerik A, Hochstrasser SM (2006) A conserved late endosome-targeting signal required for Doa4 deubiquitylating enzyme function. J Cell Biol 175:825–835

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Athalye M, Noble WC, Minnikin DE (2010) Analysis of cellular fatty acids by gas chromatography as a tool in the identification of medically important coryneform bacteria. J Appl Bacteriol 58:507–512

    Article  Google Scholar 

  • Bergmann GT, Bates ST, Eilers KG, Lauber CL, Caporaso JG, Walters WA et al (2011) The under-recognized dominance of Verrucomicrobia in soil bacterial communities. Soil Biol Biochem 43:1450–1455

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Boedeker C, Schüler M, Reintjes G, Jeske O, van Teeseling MCF et al (2017) Determining the bacterial cell biology of Planctomycetes. Nat Commun 8:14853

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cantarel BL, Coutinho PM, Corinne R et al (2009) The Carbohydrate-Active EnZymes database (CAZy): an expert resource for Glycogenomics. Nuclc Acids Res 37:D233–D238

    Article  CAS  Google Scholar 

  • Capella-Gutierrez S, Silla-Martinez JM, Gabaldon T (2009) trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics 25:1972–1973

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cayrou C, Raoult D, Drancourt M (2010) Broad-spectrum antibiotic resistance of Planctomycetes organisms determined by Etest. J Antimicrob Chemother 65:2119–2122

    Article  CAS  PubMed  Google Scholar 

  • Chiang E, Schmidt ML, Berry MA, Biddanda BA, Burtner A, Johengen TH et al (2018) Verrucomicrobia are prevalent in north-temperate freshwater lakes and display class-level preferences between lake habitats. Plos One 13(3):e0195112

    Article  PubMed  PubMed Central  Google Scholar 

  • Cho J, Vergin KL, Morris RM, Giovannoni SJ (2004) Lentisphaera araneosa gen. nov., sp. nov, a transparent exopolymer producing marine bacterium, and the description of a novel bacterial phylum. Lentisphaerae Environ Microbiol 6:611–621

    Article  CAS  PubMed  Google Scholar 

  • Cockerill F, Wikler M, Bush K, Cockerill FR (2011) Performance standards for antimicrobial susceptibility testing; twenty-first informational supplement: CLSI document M100-S21

  • Depommier C, Everard A, Druart C, Plovier H, Hul MV et al (2019) Supplementation with Akkermansia muciniphila in overweight and obese human volunteers: a proof-of-concept exploratory study. Nat Med 25:1096

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Derrien M, Vaughan EE, Plugge CM, de Vos WM (2004) Akkermansia muciniphila gen. nov., sp. nov., a human intestinal mucin-degrading bacterium. Int J Syst Evol Microbiol 54:1469–1476

    Article  CAS  PubMed  Google Scholar 

  • Edgar RC (2004) MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics 5:113

    Article  PubMed  PubMed Central  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Feng X, Zou QH, Zhang XY, Ye MQ, Du ZJ (2020) Oceanipulchritudo coccoides gen. nov., sp. Nov., isolated from marine sediment within the family Puniceicoccaceae. Int J Syst Evol Microbiol 70(11):5654–5664

    Article  CAS  PubMed  Google Scholar 

  • García-López M, Meier-Kolthoff JP, Tindall BJ, Gronow S, Woyke T et al (2019) Analysis of 1,000 type-strain genomes improves taxonomic classification of Bacteroidetes. Front Microbiol 10:2083

    Article  PubMed  PubMed Central  Google Scholar 

  • Glaeser SP, Galatis H, Martin K, Kämpfer P (2012) Luteolibacter cuticulihirudinis sp. nov., isolated from Hirudo medicinalis. Antonie Van Leeuwenhoek 102:319–324

    Article  CAS  PubMed  Google Scholar 

  • Godinho O, Calisto R, Øvreås L, Quinteira S, Lage OM (2019) Antibiotic susceptibility of marine Planctomycetes. Antonie Van Leeuwenhoek 112:1273–1280

    Article  CAS  PubMed  Google Scholar 

  • Goris J, Konstantinidis KT, Klappenbach JA, Coenye T, Vandamme P et al (2007) DNA-DNA hybridization values and their relationship to whole-genome sequence similarities. Int J Syst Evol Microbiol 57:81–91

    Article  CAS  PubMed  Google Scholar 

  • Hedlund BP, Gosink JJ, Staley JT (1997) Verrucomicrobia div. nov., a new division of the bacteria containing three new species of Prosthecobacter. Antonie Van Leeuwenhoek 72:29–38

    Article  CAS  PubMed  Google Scholar 

  • Hou S, Makarova KS, Saw JH, Senin P, Ly V, BV, et al (2008) Complete genome sequence of the extremely acidophilic methanotroph isolate V4, Methylacidiphilum infernorum, a representative of the bacterial phylum Verrucomicrobia. Biol Direct 3:26

    Article  PubMed  PubMed Central  Google Scholar 

  • Jana T, Lam-Tung N, Arndt von H, Quang MB (2016) W-IQ-TREE: a fast online phylogenetic tool for maximum likelihood analysis. Nucleic Acids Res W232–W235

  • Jenkins C, Samudrala R, Anderson I, Hedlund BP, Petroni G et al (2003) Genes for the cytoskeletal protein tubulin in the bacterial genus Prosthecobacter. Proc Natl Acad Sci 99:17049–17054

    Article  Google Scholar 

  • Jones LJ, Carballido-López R, Errington J (2001) Control of cell shape in bacteria: helical, actin-like filaments in Bacillus subtilis. Cell 104:913–922

    Article  CAS  PubMed  Google Scholar 

  • Kai B, Simon S, Alexander MK, Zach CP, Gilles PW et al (2021) antiSMASH 6.0: improving cluster detection and comparison capabilities. Nucleic Acids Res 49:W29–W35

    Article  Google Scholar 

  • Kanehisa M, Sato Y, Kawashima M, Furumichi M, Tanabe M (2016) KEGG as a reference resource for gene and protein annotation. Nucleic Acids Res 44:D457–D462

    Article  CAS  PubMed  Google Scholar 

  • Karin L, Peter H, Andreas RE, Staerfeldt HH, Rognes T et al (2007) RNAmmer: consistent and rapid annotation of ribosomal RNA genes. Nucleic Acids Res 35:3100–3108

    Article  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 

  • Kumars S, Stecher G, Tamura K (2016) MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets. Mol Biol Evol 33:1870–1874

    Article  Google Scholar 

  • Lane DJ (1991) 16S/23S rRNA sequencing. In: Stackebrandt E, Goodfellow M (eds) Nucleic Acid Tech Bact Syst. Wiley, New York, pp 115–175

    Google Scholar 

  • Lee I, Chalita M, Ha SM, Na SI, Yoon SH et al (2017) ContEst16S: an algorithm that identifies contaminated prokaryotic genomes using 16S RNA gene sequences. Int J Syst Evol Microbiol 67:2053–2057

    Article  CAS  PubMed  Google Scholar 

  • Lonhienne T, Sagulenko E, Webb RI, Lee KC, Franke J et al (2010) Endocytosis-like protein uptake in the bacterium Gemmata obscuriglobus. Proc Natl Acad Sci 107:12883–12888

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Manuel MG, Brazel DM, Swan BK, Arnosti C, Chain PSG et al (2012) Capturing single cell genomes of active polysaccharide degraders: an unexpected contribution of Verrucomicrobia. Plos One 7:e35314

    Article  Google Scholar 

  • Meuric V, Gracieux P, Tamanai-Shacoori Z, Perez-Chaparro J, Bonnaure-Mallet M et al (2010) Expression patterns of genes induced by oxidative stress in Porphyromonas gingivalis. Oral Microbiol Immunol 23:308–314

    Article  Google Scholar 

  • Minnikin DE, Minnikin SM, Goodfellow M, Stanford JL (1982) The mycolic acids of Mycobacterium chelonei. J Gen Microbiol 128:817–822

    CAS  PubMed  Google Scholar 

  • Na SI, Kim YO, Yoon SH, Ha SM, Baek I et al (2018) UBCG: Up-to-date bacterial core gene set and pipeline for phylogenomic tree reconstruction. J Microbiol 56:280–285

    Article  CAS  PubMed  Google Scholar 

  • Ogura T, Bouloc P, Niki H, D’Ari R, Hiraga S, Jaffé A (1989) Penicillin-binding protein 2 is essential in wild-type Escherichia coli but not in lov or cya mutants. J Bacteriol 171:3025–30

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Parte AC, Carbasse JS, Meier-Kolthoff JP, Reimer LC, Göker M (2020) List of Prokaryotic names with Standing in Nomenclature (LPSN) moves to the DSMZ. Int J Syst Evol Microbiol 70:5607–5612

    Article  PubMed  PubMed Central  Google Scholar 

  • Pimentel-Elardo S, Wehrl M, Friedrich AB, Schlesner H, Jensen PR et al (2003) Isolation of Planctomycetes from Aplysina sponges. Aquat Microb Ecol 33:239–245

    Article  Google Scholar 

  • Piotr S, Elzbieta DZ (2001) “Liquidless” cell staining by dye diffusion from gels and analysis by laser scanning cytometry: Potential application at microgravity conditions in space. Cytometry 44:355–360

    Article  Google Scholar 

  • Price MN, Dehal PS, Arkin AP (2010) FastTree 2-Approximately Maximum-Likelihood Trees for Large Alignments. PloS One 5:e9490

    Article  PubMed  PubMed Central  Google Scholar 

  • Qin QL, Xie BB, Zhang XY, Chen XL, Zhou BC (2014) A proposed genus boundary for the prokaryotes based on genomic insights. J Bacteriol 196:2210–2215

    Article  PubMed  PubMed Central  Google Scholar 

  • Rodriguez-R LM, Konstantinidis KT (2014) Bypassing cultivation to identify bacterial species. Microbe 9:111–118

    Google Scholar 

  • Saier MH, Tran CV, Barabote RD (2006) TCDB: the Transporter Classification Database for membrane transport protein analyses and information. Nucleic Acids Res 34:D181

    Article  CAS  PubMed  Google Scholar 

  • Sait M, Kamneva OK, Fay DS, Kirienko NV, Polek J et al (2011) Genomic and experimental evidence suggests that Verrucomicrobium spinosum interacts with eukaryotes. Front Microbiol 18(2):211

    Google Scholar 

  • Scheuermayer M, Gulder T, Bringmann G (2006) Rubritalea marina gen. nov., sp. nov., a marine representative of the phylum “Verrucomicrobia”, isolated from a sponge (Porifera). Int J Syst Evol Microbiol 56:2119–2124

    Article  CAS  PubMed  Google Scholar 

  • Simon A, Adam A, Vermeesch JR, Hestand MS (2018) Single molecule real-time (SMRT) sequencing comes of age: applications and utilities for medical diagnostics. Nucleic Acids Res 46:2159–2168

    Article  Google Scholar 

  • Spring S, Bunk B, Spröer C, Schumann P, Rohde M et al (2016) Characterization of the first cultured representative of Verrucomicrobia subdivision 5 indicates the proposal of a novel phylum. ISME J 10:2801–2816

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tatusov RL, Fedorova ND, Jackson JD, Jacobs AR, Kiryutin B et al (2003) The COG database: an updated version includes eukaryotes. BMC Bioinformatics 4:41–41

    Article  PubMed  PubMed Central  Google Scholar 

  • Vaughan S, Wickstead B, Gull K, Addinall SG (2004) Molecular evolution of FtsZ protein sequences encoded within the genomes of Archaea, Bacteria, and Eukaryota. J Mol Evol 58:19–29

    Article  CAS  PubMed  Google Scholar 

  • Wagner M, Horn M (2006) The Planctomycetes, Verrucomicrobia, Chlamydiae and sister phyla comprise a superphylum with biotechnological and medical relevance. Curr Opin Biotechnol 17:241–249

    Article  CAS  PubMed  Google Scholar 

  • Wiegand S, Jogler M, Boedeker C, Pinto D, Vollmers J et al (2020) Cultivation and functional characterization of 79 planctomycetes uncovers their unique biology. Nat Microbiol 5:126–140

    Article  CAS  PubMed  Google Scholar 

  • Yarza P, Yilmaz P, Pruesse E, Glöckner FO, Ludwig W et al (2014) Uniting the classification of cultured and uncultured bacteria and archaea using 16S rRNA gene sequences. Nat Rev Microbiol 12:635–645

    Article  CAS  PubMed  Google Scholar 

  • Yoon J, Matsuo Y, Matsuda S, Adachi K, Kasai H et al (2007) Rubritalea spongiae sp. nov. and Rubritalea tangerina sp. nov., two carotenoid- and squalene-producing marine bacteria of the family Verrucomicrobiaceae within the phylum “Verrucomicrobia”, isolated from marine animals. Int J Syst Evol Microbiol 57:2337–2343

    Article  CAS  PubMed  Google Scholar 

  • Yoon J, Matsuo Y, Katsuta A, Jang JH, Matsuda S et al (2008a) Haloferula rosea gen. nov., sp. nov., Haloferula harenae sp. nov., Haloferula phyci sp. nov., Haloferula helveola sp. nov. and Haloferula sargassicola sp. nov., five marine representatives of the family Verrucomicrobiaceae within the phylum 'Verrucomicrobia’. Int J Syst Evol Microbiol 58:2491–2500

    Article  CAS  PubMed  Google Scholar 

  • Yoon J, Matsuo Y, Adachi K, Nozawa M, Matsuda SH et al (2008b) Description of Persicirhabdus sediminis gen. nov., sp. nov., Roseibacillus ishigakijimensis gen. nov., sp. nov., Roseibacillus ponti sp. nov., Roseibacillus persicicus sp. nov., Luteolibacter pohnpeiensis gen. nov., sp. nov. and Luteolibacter algae sp. nov., six marine members of the phylum “Verrucomicrobia”, and emended descriptions of the class Verrucomicrobiae, the order Verrucomicrobiales and the family Verrucomicrobiaceae. Int J Syst Evol Microbiol 58:998–1007

    Article  PubMed  Google Scholar 

  • 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 110:1281–1286

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

Scanning electron microscopy was supported by the Physical-Chemical Materials Analytical & Testing Centre of Shandong University at Weihai. We would also like to thank Editage (www.editage.com) for English language editing.

Funding

This work was supported by the National Natural Science Foundation of China (32070002, 31770002) and National Science and Technology Fundamental Resources Investigation Program of China (2019FY100700).

Author information

Authors and Affiliations

  1. Marine College, Shandong University, Weihai, 264209, Shandong, People’s Republic of China

    Xi Feng, Qi-Yun Liang, Qi-Hang Zou, Meng-Qi Ye & Zong-Jun Du

  2. State Key Laboratory of Microbial Technology, Shandong University, Qingdao, 266237, Shandong, People’s Republic of China

    Zong-Jun Du

Authors
  1. Xi Feng
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Qi-Yun Liang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Qi-Hang Zou
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Meng-Qi Ye
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Zong-Jun Du
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

XF performed most of the experiments, wrote the main part of the manuscript, and functions as the first author. QHZ helped with the isolation of the novel strain and with cultivation measurements. MQY contributed to the literature search and analysed the sequencing data. XF and ZJD designed the study and helped with experimental setups and design.

Corresponding author

Correspondence to Zong-Jun Du.

Ethics declarations

Conflict of interest

The authors declare that the research was conducted in the absence of any commercial or financial relationships.

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 1065 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Feng, X., Liang, QY., Zou, QH. et al. Sulfuriroseicoccus oceanibius gen. nov., sp. nov., a representative of the phylum Verrucomicrobia with a special cytoplasmic membrane. Antonie van Leeuwenhoek 115, 337–352 (2022). https://doi.org/10.1007/s10482-021-01689-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10482-021-01689-2

Keywords

Search

Navigation