Skip to main content
SpringerLink
Log in

Description of Flavimaribacter sediminis gen. nov., sp. nov., a New Member of the Family Rhizobiaceae Isolated from Marine Sediment

  • Published:
Current Microbiology Aims and scope Submit manuscript

Abstract

A novel Gram-staining-negative, aerobic and rod-shaped bacterium, designated WL0058T, was isolated from coastal sediment sample collected in Nantong city, Jiangsu province of China (120° 51′ 13″ E, 32° 6′ 26″ N) in October 2020. Strain WL0058T was found to grow at 4–37 °C (optimum, 28 °C) with 1.5–4.0% NaCl (optimum, 4.0%) and displayed alkaliphilic growth with the pH range of pH 6.0–10.0 (optimum, pH 6.0). Phylogenetic trees constructed based on 16S rRNA gene sequence indicated that strain WL0058T is a member of the family Rhizobiaceae, shared the highest similarity with “Hoeflea prorocentri” CCTCC AB 2016294T (97.7%) and constituted a sub-cluster within the family with it, while the similarity with others in the family Rhizobiaceae was lower than 97.0%. The G + C content of genomic DNA was 59.5 mol%. Polar lipids profile of strain WL0058T included phosphatidylcholine (PC), phosphatidylethanolamine (PE), and glycolipid (GL), phosphatidylmonomethylethanolamine (PME) and two unidentified polar lipids (L). The major isoprenoid quinone was determined to be Q-10 and the major fatty acids were C16:0, C18:0, summed features 4 (iso-C17:1 and/or anteiso-C17:1), and summed features 8 (C18:1ω6c and/or C18:1ω7c). As inferred from the morphology, physiology, and biochemical analysis, genotypic characteristics, and the phylogenetic trees, strain WL0058T ought to be recognized as a novel genus in the family Rhizobiaceae, for which the name Flavimaribacter sediminis gen. nov., sp. nov. The type strain of Flavimaribacter sediminis gen. nov., sp. nov. is WL0058T (= MCCC 1K06063T = JCM 34659T = GDMCC 1.2448T).

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

Similar content being viewed by others

Data Availability

All of the data supporting the conclusions of this article are included within the article and its additional files. The genome datasets and the 16S rRNA gene sequence of Flavimaribacter sediminis WL0058T and “Hoeflea prorocentri” CCTCC AB 2016294T generated during the current study are available in the GenBank/EMBL/DDBJ repository under accession number JAICBX000000000 and OP592206, JAPPVY000000000 and KY264918, respectively. Other datasets used and/or analyzed during the current study are available from the corresponding author upon reasonable request. Other genome sequence data detailed information is listed in Table S1.

References

  1. Conn H (1938) Taxonomic relationships of certain non-sporeforming rods in soil. J Bacteriol 36:320–321

    Google Scholar 

  2. Douglas H (1957) Order III. Hyphomicrobiales Douglas, ordo nov. Bergey’s manual of determinative bacteriology: pp. 276–280.

  3. Garrity GM, Bell JA, Lilburn T (2005) Class I. Alphaproteobacteria class. nov. In: Shalu V (ed) Bergey’s manual of systematic bacteriology. Springer, Berlin, pp 1–1

    Google Scholar 

  4. Parte AC (2018) LPSN – list of prokaryotic names with standing in nomenclature (bacterio.net), 20 years on. Int J Syst Evol Microbiol 68:1825–1829. https://doi.org/10.1099/ijsem.0.002786

    Article  PubMed  Google Scholar 

  5. Conn HJ (1942) Validity of the genus Alcaligenes. J Bacteriol 44:353–360. https://doi.org/10.1128/jb.44.3.353-360.1942

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. de Lajudie P, Laurent-Fulele E, Willems A, Torck U, Coopman R, Collins MD, Kersters K, Dreyfus B, Gillis M (1998) Allorhizobium undicola gen. nov., sp. nov., nitrogen-fixing bacteria that efficiently nodulate Neptunia natans in Senegal. Int J Syst Bacteriol 48:1277–1290. https://doi.org/10.1099/00207713-48-4-1277

    Article  PubMed  Google Scholar 

  7. Kathiravan R, Jegan S, Ganga V, Prabavathy VR, Tushar L, Sasikala C, Ramana CV (2013) Ciceribacter lividus gen. nov., sp. nov., isolated from rhizosphere soil of chick pea (Cicer arietinum L.). Int J Syst Evol Microbiol 63:4484–4488. https://doi.org/10.1099/ijs.0.049726-0

    Article  CAS  PubMed  Google Scholar 

  8. Menéndez E, Flores-Félix JD, Ramírez-Bahena MH, Igual JM, García-Fraile P, Peix A, Velázquez E (2020) Genome analysis of Endobacterium cerealis, a novel genus and species isolated from Zea mays Roots in North Spain. Microorganisms 8:939. https://doi.org/10.3390/microorganisms8060939

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Casida LE (1982) Ensifer adhaerens gen. nov., sp. nov.: a bacterial predator of bacteria in soil. Int J Syst Evol Microbiol 32:339–345. https://doi.org/10.1099/00207713-32-3-339

    Article  Google Scholar 

  10. Tóth E, Szuróczki S, Kéki Z, Bóka K, Szili-Kovács T, Schumann P (2017) Gellertiella hungarica gen. nov., sp. nov., a novel bacterium of the family Rhizobiaceae isolated from a spa in Budapest. Int J Syst Evol Microbiol 67:4565–4571. https://doi.org/10.1099/ijsem.0.002332

    Article  CAS  PubMed  Google Scholar 

  11. Cao J, Wei Y, Lai Q, Wu Y, Deng J, Li J, Liu R, Wang L, Fang J (2020) Georhizobium profundi gen. nov., sp. nov., a piezotolerant bacterium isolated from a deep-sea sediment sample of the New Britain Trench. Int J Syst Evol Microbiol 70:373–379. https://doi.org/10.1099/ijsem.0.003766

    Article  CAS  PubMed  Google Scholar 

  12. Peix A, Rivas R, Trujillo ME, Vancanneyt M, Velázquez E, Willems A (2005) Reclassification of Agrobacterium ferrugineum LMG 128 as Hoeflea marina gen. nov., sp. nov. Int J Syst Evol Microbiol 55:1163–1166. https://doi.org/10.1099/ijs.0.63291-0

    Article  CAS  PubMed  Google Scholar 

  13. Park S, Lee JS, Lee KC, Yoon JH (2013) Lentilitoribacter donghaensis gen. nov., sp. nov., a slowly-growing alphaproteobacterium isolated from coastal seawater. Antonie Van Leeuwenhoek 103:457–464. https://doi.org/10.1007/s10482-012-9825-9

    Article  PubMed  Google Scholar 

  14. Fagen JR, Leonard MT, Coyle JF, McCullough CM, Davis-Richardson AG, Davis MJ, Triplett EW (2014) Liberibacter crescens gen. nov., sp. nov., the first cultured member of the genus Liberibacter. Int J Syst Evol Microbiol 64:2461–2466. https://doi.org/10.1099/ijs.0.063255-0

    Article  CAS  PubMed  Google Scholar 

  15. Rivas R, Sánchez-Márquez S, Mateos PF, Martínez-Molina E, Velázquez E (2005) Martelella mediterranea gen. nov., sp. nov., a novel alpha-proteobacterium isolated from a subterranean saline lake. Int J Syst Evol Microbiol 55:955–959. https://doi.org/10.1099/ijs.0.63438-0

    Article  CAS  PubMed  Google Scholar 

  16. Gray P, Thornton H (1928) Soil bacteria that decompose certain aromatic compounds. Zentralbl Bakteriol Parasitenk Infektionsk 73:74–96

    CAS  Google Scholar 

  17. Mousavi SA, Österman J, Wahlberg N, Nesme X, Lavire C, Vial L, Paulin L, de Lajudie P, Lindström K (2014) Phylogeny of the Rhizobium-Allorhizobium-Agrobacterium clade supports the delineation of Neorhizobium gen. nov. Syst Appl Microbiol 37:208–215. https://doi.org/10.1016/j.syapm.2013.12.007

    Article  CAS  PubMed  Google Scholar 

  18. Mousavi SA, Willems A, Nesme X, de Lajudie P, Lindström K (2015) Revised phylogeny of Rhizobiaceae: proposal of the delineation of Pararhizobium gen. nov., and 13 new species combinations. Syst Appl Microbiol 38:84–90. https://doi.org/10.1016/j.syapm.2014.12.003

    Article  PubMed  Google Scholar 

  19. Kimes NE, López-Pérez M, Flores-Félix JD, Ramírez-Bahena MH, Igual JM, Peix A, Rodriguez-Valera F, Velázquez E (2015) Pseudorhizobium pelagicum gen. nov., sp. nov. isolated from a pelagic Mediterranean zone. Syst Appl Microbiol 38:293–299. https://doi.org/10.1016/j.syapm.2015.05.003

    Article  PubMed  Google Scholar 

  20. Frank B (1889) Über die Pilzsymbiose der Leguminosen. Berichte Deutschen Botanischen Gesellschaft.

  21. An DS, Im WT, Yang HC, Lee ST (2006) Shinella granuli gen. nov., sp. nov., and proposal of the reclassification of Zoogloea ramigera ATCC 19623 as Shinella zoogloeoides sp. nov. Int J Syst Evol Microbiol 56:443–448. https://doi.org/10.1099/ijs.0.63942-0

    Article  CAS  PubMed  Google Scholar 

  22. Hördt A, López MG, Meier-Kolthoff JP, Schleuning M, Weinhold LM, Tindall BJ, Gronow S, Kyrpides NC, Woyke T, Göker M (2020) Analysis of 1,000+ type-strain genomes substantially improves taxonomic classification of Alphaproteobacteria. Front Microbiol 11:468. https://doi.org/10.3389/fmicb.2020.00468

    Article  PubMed  PubMed Central  Google Scholar 

  23. Weisburg WG, Barns SM, Pelletier DA, Lane DJ (1991) 16S ribosomal DNA amplification for phylogenetic study. J Bacteriol 173:697–703. https://doi.org/10.1128/jb.173.2.697-703.1991

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. 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. https://doi.org/10.1099/ijsem.0.001755

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Yang Q, Jiang Z-W, Huang C-H, Zhang R-N, Li L-Z, Yang G, Feng L-J, Yang G-F, Zhang H, Zhang X-L, Mu J (2018) Hoeflea prorocentri sp. nov., isolated from a culture of the marine dinoflagellate Prorocentrum mexicanum PM01. Antonie Van Leeuwenhoek 111:1845–1853. https://doi.org/10.1007/s10482-018-1074-0

    Article  CAS  PubMed  Google Scholar 

  26. Chung EJ, Park JA, Pramanik P, Bibi F, Jeon CO, Chung YR (2013) Hoeflea suaedae sp. nov., an endophytic bacterium isolated from the root of the halophyte Suaeda maritima. Int J Syst Evol Microbiol 63:2277–2281. https://doi.org/10.1099/ijs.0.045484-0

    Article  CAS  PubMed  Google Scholar 

  27. Hyeon JW, Jeong SE, Baek K, Jeon C (2017) Roseitalea porphyridii gen. nov., sp. nov., isolated from a red alga, and reclassification of Hoeflea suaedae Chung 2013 as Pseudohoeflea suaedae gen. nov., comb. nov. Int J Syst Evol Microbiol 67:362–368. https://doi.org/10.1099/ijsem.0.001633

    Article  CAS  PubMed  Google Scholar 

  28. Johnson M, Zaretskaya I, Raytselis Y, Merezhuk Y, McGinnis S, Madden TL (2008) NCBI BLAST: a better web interface. Nucleic Acids Res. https://doi.org/10.1093/nar/gkn201

    Article  PubMed  PubMed Central  Google Scholar 

  29. Nurk S, Bankevich A, Antipov D, Gurevich AA, Korobeynikov A, Lapidus A, Prjibelski AD, Pyshkin A, Sirotkin A, Sirotkin Y, Stepanauskas R, Clingenpeel SR, Woyke T, McLean JS, Lasken R, Tesler G, Alekseyev MA, Pevzner PA (2013) Assembling single-cell genomes and mini-metagenomes from chimeric MDA products. J Comput Biol 20:714–737. https://doi.org/10.1089/cmb.2013.0084

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Okonechnikov K, Golosova O, Fursov M, Team U (2012) Unipro UGENE: a unified bioinformatics toolkit. Bioinformatics 28:1166–1167. https://doi.org/10.1093/bioinformatics/bts091

    Article  CAS  PubMed  Google Scholar 

  31. Goris J, Konstantinidis KT, Klappenbach JA, Coenye T, Vandamme P, Tiedje JM (2007) DNA–DNA hybridization values and their relationship to whole-genome sequence similarities. Int J Syst Evol Microbiol 57:81–91. https://doi.org/10.1099/ijs.0.64483-0

    Article  CAS  PubMed  Google Scholar 

  32. Richter M, Rosselló-Móra R (2009) Shifting the genomic gold standard for the prokaryotic species definition. Proc Natl Acad Sci U S A 106:19126–19131. https://doi.org/10.1073/pnas.0906412106

    Article  PubMed  PubMed Central  Google Scholar 

  33. Rodriguez-R LM, Konstantinidis KT (2016) The enveomics collection: a toolbox for specialized analyses of microbial genomes and metagenomes. PeerJ Preprints. https://doi.org/10.7287/peerj.preprints.1900v1

    Article  Google Scholar 

  34. 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 196:2210–2215. https://doi.org/10.1128/jb.01688-14

    Article  PubMed  PubMed Central  Google Scholar 

  35. Meier-Kolthoff JP, Auch AF, Klenk HP, Göker M (2013) Genome sequence-based species delimitation with confidence intervals and improved distance functions. BMC Bioinformatics 14:60. https://doi.org/10.1186/1471-2105-14-60

    Article  PubMed  PubMed Central  Google Scholar 

  36. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Huerta-Cepas J, Forslund K, Coelho LP, Szklarczyk D, Jensen LJ, von Mering C, Bork P (2017) Fast genome-wide functional annotation through orthology assignment by eggNOG-Mapper. Mol Biol Evol 34:2115–2122. https://doi.org/10.1093/molbev/msx148

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. 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:D457-462. https://doi.org/10.1093/nar/gkv1070

    Article  CAS  PubMed  Google Scholar 

  39. Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425. https://doi.org/10.1093/oxfordjournals.molbev.a040454

    Article  CAS  PubMed  Google Scholar 

  40. Rzhetsky A, Nei M (1992) A simple method for estimating and testing minimum-evolution trees. Mol Biol Evol 9:945–945. https://doi.org/10.1093/oxfordjournals.molbev.a040771

    Article  CAS  Google Scholar 

  41. Fitch WM (1971) Toward defining the course of evolution: minimum change for a specific tree topology. Syst Zool 20:406–416. https://doi.org/10.2307/2412116

    Article  Google Scholar 

  42. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. 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. https://doi.org/10.1007/bf01731581

    Article  CAS  PubMed  Google Scholar 

  44. Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791. https://doi.org/10.1111/j.1558-5646.1985.tb00420.x

    Article  PubMed  Google Scholar 

  45. Zhang DF, Cui XW, Zhao Z, Zhang AH, Huang JK, Li WJ (2020) Sphingomonas hominis sp. nov., isolated from hair of a 21-year-old girl. Antonie Van Leeuwenhoek 113:1523–1530. https://doi.org/10.1007/s10482-020-01460-z

    Article  CAS  PubMed  Google Scholar 

  46. Huson DH, Bryant D (2005) Application of phylogenetic networks in evolutionary studies. Mol Biol Evol 23:254–267. https://doi.org/10.1093/molbev/msj030

    Article  CAS  PubMed  Google Scholar 

  47. Sasser M (1990) Identification of bacteria by gas chromatography of cellular fatty acids. USFCC Newsl 20:1–6

    Google Scholar 

  48. 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. https://doi.org/10.1111/j.1365-2672.1980.tb01036.x

    Article  CAS  Google Scholar 

  49. Minnikin DE, O’Donnell AG, Goodfellow M, Alderson G, Athalye M, Schaal A, Parlett JH (1984) An integrated procedure for the extraction of bacterial isoprenoid quinones and polar lipids. J Microbiol Methods 2:233–241. https://doi.org/10.1016/0167-7012(84)90018-6

    Article  CAS  Google Scholar 

  50. Collins MD, Pirouz T, Goodfellow M, Minnikin DE (1977) Distribution of menaquinones in actinomycetes and corynebacteria. J Gen Microbiol 100:221–230. https://doi.org/10.1099/00221287-100-2-221

    Article  CAS  PubMed  Google Scholar 

  51. Tamaoka J (1986) Analysis of bacterial menaquinone mixtures by reverse-phase high-performance liquid chromatography. Methods Enzymol 123:251–256. https://doi.org/10.1016/s0076-6879(86)23028-1

    Article  CAS  PubMed  Google Scholar 

  52. Rodríguez-R L, Konstantinidis KT (2014) Bypassing cultivation to identify bacterial species. Microbe 9:111–118. https://doi.org/10.1128/microbe.9.111.1

    Article  Google Scholar 

  53. Ramírez-Bahena MH, García-Fraile P, Peix A, Valverde A, Rivas R, Igual JM, Mateos PF, Martínez-Molina E, Velázquez E (2008) Revision of the taxonomic status of the species Rhizobium leguminosarum (Frank 1879) Frank 1889AL, Rhizobium phaseoli Dangeard 1926AL and Rhizobium trifolii Dangeard 1926AL. R. trifolii is a later synonym of R. leguminosarum. Reclassification of the strain R. leguminosarum DSM 30132 (=NCIMB 11478) as Rhizobium pisi sp. nov. Int J Syst Evol Microbiol 58:2484–2490. https://doi.org/10.1099/ijs.0.65621-0

    Article  CAS  PubMed  Google Scholar 

  54. Amarger N, Macheret V, Laguerre G (1997) Rhizobium gallicum sp. nov. and Rhizobium giardinii sp. nov., from Phaseolus vulgaris nodules. Int J Syst Bacteriol 47:996–1006. https://doi.org/10.1099/00207713-47-4-996

    Article  CAS  PubMed  Google Scholar 

  55. Naqvi SU, Qin Y, Tahir A, Stougaard P (2017) Pararhizobium antarcticum sp. nov., isolated from Antarctic water samples. Int J Syst Evol Microbiol 67:1650–1655. https://doi.org/10.1099/ijsem.0.001828

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The authors are grateful to Prof. Aharon Oren (The Hebrew University of Jerusalem, Israel) for helping with the etymology.

Funding

This research was supported by the Innovation Project for Marine Science and Technology of Jiangsu Province (No. JSZRHYKJ202209) and the China Postdoctoral Science Foundation (2020M671312).

Author information

Author notes

  1. Xiang-Ning Wang and Lu Wang have contributed equally to this work.

Authors and Affiliations

  1. Nanjing Forestry University, Nanjing, 210037, People’s Republic of China

    Xiang-Ning Wang & Lu Wang

  2. Institute of Marine Biotechnology and Bio-resource Utilization, College of Oceanography, Hohai University, Nanjing, 201198, People’s Republic of China

    Lu Wang, Wei He & Dao-Feng Zhang

  3. Laboratory of Marine Environment and Ecology, College of Marine Science and Technology, Zhejiang Ocean University, Zhoushan, 316022, People’s Republic of China

    Qiao Yang

Authors
  1. Xiang-Ning Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Lu Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Wei He
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Qiao Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Dao-Feng Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

X-NW and D-FZ designed research and project outline. LW and WH performed isolation, deposition and polyphasic taxonomy. WH performed genome analysis. WH, QY, and X-NW drafted the manuscript. WH and D-FZ revised the manuscript. All authors read and approved the final manuscript.

Corresponding authors

Correspondence to Xiang-Ning Wang or Dao-Feng Zhang.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical Approval

This article does not contain any studies with human participants or animals performed by any of the authors. The authors have declared that no ethical issues exist.

Research Involving Human and/or Animal Participants

This article does not contain any studies with human participants or animals performed by any of the authors.

Consent for Publication

All authors agree to have participated in the research proposed to be published and agree to be published in the journal.

Consent to Participate

Not applicable.

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 9474 KB)

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.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wang, XN., Wang, L., He, W. et al. Description of Flavimaribacter sediminis gen. nov., sp. nov., a New Member of the Family Rhizobiaceae Isolated from Marine Sediment. Curr Microbiol 80, 301 (2023). https://doi.org/10.1007/s00284-023-03402-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00284-023-03402-0

Search

Navigation