1887

INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY logo

Volume 71, Issue 7

gen. nov., sp. nov., a moderately halophilic bacterium isolated from bioturbated Red Sea mangrove sediment, and proposal of the novel family fam. nov. Open Access

Abstract

A strictly aerobic, Gram-stain-negative, non-motile, rod-shaped bacterium, designated strain R1DC9, was isolated from sediments of a mangrove stand on the Red Sea coast of Saudi Arabia via diffusion chamber cultivation. Strain R1DC9 grew at 20–40 °C (optimum, 37 °C), pH 6–10 (optimum, pH 8) and 3–11 % NaCl (optimum, 7–9 %) in the cultivation medium. The genome of R1DC9 was 4 661 901 bp long and featured a G+C content of 63.1 mol%. Phylogenetic analyses based on the 16S rRNA gene sequence and whole-genome multilocus sequence analysis using 120 concatenated single-copy genes revealed that R1DC9 represents a distinct lineage in the order and the phylum separated from the and families. R1DC9 displayed 90 and 89 % 16S rRNA gene sequence identities with DSM 4125 and KMM 6017, respectively. The predominant quinone was MK7. The polar lipids were phosphatidylethanolamine, two unknown phospholipids and two unknown lipids. The predominant cellular fatty acids were the saturated branch chain fatty acids iso-C, iso-C 3-OH and iso-C, along with a low percentage of the monounsaturated fatty acid C 5. Based on differences in phenotypic, physiological and biochemical characteristics from known relatives, and the results of phylogenetic analyses, R1DC9 (=KCTC 72349=JCM 33609=NCCB 100698) is proposed to represent a novel species in a new genus, and the name gen. nov., sp. nov. is proposed. The distinct phylogenetic lineage among the families in the order indicates that R1DC9 represents a new family for which the name fam. nov. is proposed.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): Bacteroidetes , cultivation , mangrove crabs , mangrove sediments , Mangrovivirga and Mangrovivirgaceae
Funding
This study was supported by the:
  • King Abdullah University of Science and Technology (Award REI/1/4483-01-01)
    • Principle Award Recipient: DanieleDaffonchio
  • King Abdullah University of Science and Technology (Award FCC/1/1973-56-01)
    • Principle Award Recipient: DanieleDaffonchio
© 2021 The Authors
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License.
Loading

Article metrics loading...

/content/journal/ijsem/10.1099/ijsem.0.004866
2021-07-02
2024-04-19
Loading full text...

Full text loading...

/deliver/fulltext/ijsem/71/7/ijsem004866.html?itemId=/content/journal/ijsem/10.1099/ijsem.0.004866&mimeType=html&fmt=ahah

References

  1. Sheaves M. Consequences of ecological connectivity: the coastal ecosystem mosaic. Mar Ecol Prog Ser 2009; 391:107–115 [View Article]
     [Google Scholar]
  2. Donato DCC, Kauffman JBB, Murdiyarso D, Kurnianto S, Stidham M et al. Mangroves among the most carbon-rich forests in the tropics. Nat Geosci 2011; 4:293–297 [View Article]
     [Google Scholar]
  3. Pramanik A, Sengupta S, Bhattacharyya M. Microbial diversity and community analysis of the Sundarbans mangrove, a world heritage site. In Microbial Diversity in the Genomic Era Academic Press; 2019 pp 65–76
     [Google Scholar]
  4. Alongi DM. Mangrove-microbe-soil relations. Kristensen E, Haese R, Kostka J. eds In Interactions Between Macro‐ and Microorganisms in Marine Sediments 2005 pp 85–103
     [Google Scholar]
  5. Santana CO, Spealman P, Melo VMM, Gresham D, Jesus TB et al. Microbial community structure and ecology in sediments of a pristine mangrove forest. bioRxiv 2019814–833
     [Google Scholar]
  6. Booth JM, Fusi M, Marasco R, Mbobo T, Daffonchio D. Fiddler crab bioturbation determines consistent changes in bacterial communities across contrasting environmental conditions. Sci Rep 2019; 9:3749 [View Article] [PubMed]
     [Google Scholar]
  7. Booth JM, Fusi M, Marasco R, Michoud G, Fodelianakis S et al. The role of fungi in heterogeneous sediment microbial networks. Sci Rep 2019; 9:7537
     [Google Scholar]
  8. Soldan R, Mapelli F, Crotti E, Schnell S, Daffonchio D et al. Bacterial endophytes of mangrove propagules elicit early establishment of the natural host and promote growth of cereal crops under salt stress. Microbiol Res 2019; 223–225:33–43
     [Google Scholar]
  9. Liu Y-L, Meng D, Li R-R, Gu P-F, Fan X-Y et al. Rhodoligotrophos defluvii sp. nov., isolated from activated sludge. Int J Syst Evol Microbiol 20193830–3836
     [Google Scholar]
  10. Al-Amoudi S, Razali R, Essack M, Amini MS, Bougouffa S et al. Metagenomics as a preliminary screen for antimicrobial bioprospecting. Gene 2016; 594:248–258 [View Article] [PubMed]
     [Google Scholar]
  11. Alonso-Sáez L, Gasol JM. Seasonal variations in the contributions of different bacterial groups to the uptake of low-molecular-weight compounds in northwestern Mediterranean coastal waters. Appl Environ Microbiol 2007; 73:3528–3535 [View Article] [PubMed]
     [Google Scholar]
  12. Pommier T, Canback B, Riemann L, Bostrom KH, Simu K et al. Global patterns of diversity and community structure in marine bacterioplankton. Mol Ecol 2006; 16:867–880 [View Article]
     [Google Scholar]
  13. Huo Y-Y, Xu L, Wang C-S, Yang J-Y, You H et al. Fabibacter pacificus sp. nov., a moderately halophilic bacterium isolated from seawater. Int J Syst Evol Microbiol 2013; 63:3710–3714 [View Article] [PubMed]
     [Google Scholar]
  14. Lin C-Y, Zhang X-Y, Liu A, Liu C, Song X-Y et al. Marivirga atlantica sp. nov., isolated from seawater and emended description of the genus Marivirga. Int J Syst Evol Microbiol 2015; 65:1515–1519 [View Article] [PubMed]
     [Google Scholar]
  15. Ludwig W, Euzéby J, Whitman WB. Road map of the phyla Bacteroidetes, Spirochaetes, Tenericutes (Mollicutes), Acidobacteria, Fibrobacteres, Fusobacteria, Dictyoglomi, Gemmatimonadetes, Lentisphaerae, Verrucomicrobia, Chlamydiae, and Planctomycetes. In Bergey’s Manual of Systematic Bacteriology New York, NY: Springer New York; 2010 pp 1–19
     [Google Scholar]
  16. Nedashkovskaya OI, Kim SB, Lysenko AM, Park MS, Mikhailov VV et al. Roseivirga echinicomitans sp. nov., a novel marine bacterium isolated from the sea urchin Strongylocentrotus intermedius, and emended description of the genus Roseivirga. Int J Syst Evol Microbiol 2005; 55:1797–1800 [View Article] [PubMed]
     [Google Scholar]
  17. Nedashkovskaya OI, Vancanneyt M, Kim SB, Bae KS. Reclassification of Flexibacter tractuosus (Lewin 1969) Leadbetter 1974 and ‘Microscilla sericea’ Lewin 1969 in the genus Marivirga gen. nov. as Marivirga tractuosa comb. nov. and Marivirga sericea nom. rev., comb. nov. Int J Syst Evol Microbiol 2010; 60:1858–1863 [View Article] [PubMed]
     [Google Scholar]
  18. Lau S, Tsoi MMY, Li X, Plakhotnikova I, Dobretsov S et al. Description of Fabibacter halotolerans gen. nov., sp. nov. and Roseivirga spongicola sp. nov., and reclassification of [Marinicola] seohaensis as Roseivirga seohaensis comb. nov. Int J Syst Evol Microbiol 2006; 56:1059–1065 [View Article] [PubMed]
     [Google Scholar]
  19. Naas AE, Solden LM, Norbeck AD, Brewer H, Hagen LH et al. "Candidatus Paraporphyromonas polyenzymogenes” encodes multi-modular cellulases linked to the type IX secretion system. Microbiome 2018; 6:44 [View Article] [PubMed]
     [Google Scholar]
  20. García-López M, Meier-Kolthoff JP, Tindall BJ, Gronow S, Woyke T et al. Analysis of 1,000 type-strain genomes improves taxonomic classification of Bacteroidetes. Front Microbiol 2019; 10:2083 [View Article] [PubMed]
     [Google Scholar]
  21. Oren A, Garrity GM. List of new names and new combinations previously effectively, but not validly, published. Int J Syst Evol Microbiol 2020; 70:2960–2966 [View Article] [PubMed]
     [Google Scholar]
  22. Khan ST, Nakagawa Y, Harayama S. Sediminitomix flava gen. nov., sp. nov., of the phylum Bacteroidetes, isolated from marine sediment. Int J Syst Evol Microbiol 2007; 57:1689–1693 [View Article] [PubMed]
     [Google Scholar]
  23. Lau KWK, Ren J, Wai NLM, Qian PY, Wong PK et al. Lishizhenia caseinilytica gen. nov., sp. nov., a marine bacterium of the phylum Bacteroidetes. Int J Syst Evol Microbiol 2006; 56:2317–2322
     [Google Scholar]
  24. Vaisman N, Oren A. Salisaeta longa gen. nov., sp. nov., a red, halophilic member of the Bacteroidetes. Int J Syst Evol Microbiol 2009; 59:2571–2574 [View Article] [PubMed]
     [Google Scholar]
  25. Sun L, Toyonaga M, Ohashi A, Tourlousse DM, Matsuura N et al. Lentimicrobium saccharophilum gen. nov., sp. nov., a strictly anaerobic bacterium representing a new family in the phylum Bacteroidetes, and proposal of Lentimicrobiaceae fam. nov. Int J Syst Evol Microbiol 2016; 66:2635–2642 [View Article] [PubMed]
     [Google Scholar]
  26. Kaeberlein T, Lewis K, Epstein SS. Isolating “uncultivable” microorganisms in pure culture in a simulated natural environment. Science 2002; 296:1127–1129 [View Article] [PubMed]
     [Google Scholar]
  27. Bollmann A, Lewis K, Epstein SS. Incubation of environmental samples in a diffusion chamber increases the diversity of recovered isolates. Appl Environ Microbiol 2007; 73:6386–6390 [View Article] [PubMed]
     [Google Scholar]
  28. Chin C-S, Alexander DH, Marks P, Klammer AA, Drake J et al. Nonhybrid, finished microbial genome assemblies from long-read SMRT sequencing data. Nat Methods 2013; 10:563–569 [View Article] [PubMed]
     [Google Scholar]
  29. Seemann T. Prokka: rapid prokaryotic genome annotation. Bioinformatics 2014; 30:2068–2069 [View Article] [PubMed]
     [Google Scholar]
  30. Bertini I, Hu X, Luchinat C. Global metabolomics characterization of bacteria: pre-analytical treatments and profiling. Metabolomics 2014; 10:241–249 [View Article]
     [Google Scholar]
  31. Aziz RK, Bartels D, Best A, DeJongh M, Disz T et al. The RAST Server: Rapid annotations using subsystems technology. BMC Genomics 2008; 9:75 [View Article] [PubMed]
     [Google Scholar]
  32. Kanehisa M, Sato Y, Kawashima M, Furumichi M, Tanabe M. KEGG as a reference resource for gene and protein annotation. Nucleic Acids Res 2016; 44:D457–D462 [View Article]
     [Google Scholar]
  33. Kumar S, Stecher G, Tamura K, Dudley J. Mega7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 2016; 33:1870–1874
     [Google Scholar]
  34. Chaumeil PA, Mussig AJ, Hugenholtz P, Parks DH. GTDB-Tk: A toolkit to classify genomes with the Genome Taxonomy Database. Bioinformatics 2020; 36:1925–1927
     [Google Scholar]
  35. Felsenstein J. Confidence limits on phylogenies: An approach using the bootstrap. Evolution 1985; 39:783–791 [View Article] [PubMed]
     [Google Scholar]
  36. Richter M, Rosselló-Móra R, Oliver Glöckner F, Peplies J. JSpeciesWS: a web server for prokaryotic species circumscription based on pairwise genome comparison. Bioinformatics 2016; 32:929–931 [View Article] [PubMed]
     [Google Scholar]
  37. Burall LS, Grim CJ, Mammel MK, Datta AR. Whole genome sequence analysis using Jspecies tool establishes clonal relationships between Listeria monocytogenes strains from epidemiologically unrelated listeriosis outbreaks. PLoS One 2016; 11:e0150797 [View Article] [PubMed]
     [Google Scholar]
  38. Meier-Kolthoff JP, Auch AF, Klenk HP, Göker M. Genome sequence-based species delimitation with confidence intervals and improved distance functions. BMC Bioinformatics 2013; 14:60 [View Article] [PubMed]
     [Google Scholar]
  39. Medlar AJ, Törönen P, Holm L. AAI-profiler: fast proteome-wide exploratory analysis reveals taxonomic identity, misclassification and contamination. Nucleic Acids Res 2018; 46:W479–W485 [View Article] [PubMed]
     [Google Scholar]
  40. Moore WEC, Stackebrandt E, Kandler O, Colwell RR, Krichevsky MI et al. Report of the Ad Hoc committee on Reconciliation of approaches to bacterial systematics. Int J Syst Evol Microbiol 1987; 37:463–464 [View Article]
     [Google Scholar]
  41. Konstantinidis KT, Rosselló-Móra R, Amann R. Uncultivated microbes in need of their own taxonomy. ISME J 2017; 11:2399–2406 [View Article] [PubMed]
     [Google Scholar]
  42. Madigan MT, Martinko JM, Dunlap P, Clark DP. Measuring microbial growth. Brock Biol Microorg 2008; 11:128–132
     [Google Scholar]
  43. Tittsler RP, Sandholzer LA. The use of semi-solid agar for the detection of bacterial motility. J Bacteriol 1936; 31:575–580 [View Article] [PubMed]
     [Google Scholar]
  44. Jain A, Jain R, Jain S. Motility testing – hanging drop method and stab. In Basic Techniques in Biochemistry, Microbiology and Molecular Biology New York: Humana; 2020 pp 121–122
     [Google Scholar]
  45. Aladame N. Bergey’s manual of systematic bacteriology: vol. 2 (J.G. Holt & P.H.A. Sneath), 1 vol. (22×28,5 cm), 1599 + xix pages. Williams & Wilkins, Baltimore, London, 1986. Annales de l’Institut Pasteur / Microbiologieannales de l’Institut Pasteur / Microbiologie 1987; 138:146
     [Google Scholar]
  46. Marasco R, Rolli E, Ettoumi B, Vigani G, Mapelli F et al. A drought resistance-promoting microbiome is selected by root system under desert farming. PLoS One 2012; 7:e48479 [View Article] [PubMed]
     [Google Scholar]
  47. Bric JM, Bostock RM, Silverstone SE. Rapid in situ assay for indoleacetic acid production by bacteria immobilized on a nitrocellulose membrane. Appl Environ Microbiol 1991; 57:535–538 [View Article] [PubMed]
     [Google Scholar]
  48. Zhu D, Niu L, Wang C, Nagata S. Isolation and characterisation of moderately halophilic bacterium Halomonas ventosae DL7 synthesizing ectoine as compatible solute. Ann Microbiol 2007; 57:401–406 [View Article]
     [Google Scholar]
  49. Arshad M, Eid EM, Hasan M. Mangrove health along the hyper-arid southern Red Sea coast of Saudi Arabia. Environ Monit Assess 2020; 192:189 [View Article] [PubMed]
     [Google Scholar]
  50. Spaepen S, Vanderleyden J. Auxin and plant-microbe interactions. Cold Spring Harb Perspect Biol 2011; 3:a001438 [View Article] [PubMed]
     [Google Scholar]
  51. Li G, Young KD. Indole production by the tryptophanase TnaA in Escherichia coli is determined by the amount of exogenous tryptophan. Microbiology (Reading) 2013; 159:402–410 [View Article] [PubMed]
     [Google Scholar]
  52. Bjursell MK, Martens EC, Gordon JI. Functional genomic and metabolic studies of the adaptations of a prominent adult human gut symbiont, Bacteroides thetaiotaomicron, to the suckling period. J Biol Chem 2006; 281:36269–36279 [View Article] [PubMed]
     [Google Scholar]
  53. Xu Z, Sun H, Jiang X, Sun H, Dang X et al. Glycinebetaine biosynthesis in response to osmotic stress depends on jasmonate signaling in watermelon suspension cells. Front Plant Sci 2018; 9:1469 [View Article] [PubMed]
     [Google Scholar]
  54. Oren A. Microbial life at high salt concentrations: phylogenetic and metabolic diversity. Saline Syst 2008; 4:2 [View Article] [PubMed]
     [Google Scholar]
  55. Gasteiger E, Hoogland C, Gattiker A, Duvaud S, Wilkins MR et al. Protein identification and analysis tools on the ExPASy server. In The Proteomics Protocols Handbook pp 571–607
     [Google Scholar]
  56. Spring S, Nolan M, Lapidus A, Glavina Del Rio T, Copeland A et al. Complete genome sequence of Desulfohalobium retbaense type strain (HR(100. Stand Genomic Sci 2010; 2:38–48 [View Article] [PubMed]
     [Google Scholar]
  57. Antón J, Oren A, Benlloch S, Rodríguez-Valera F, Amann R et al. Salinibacter ruber gen. nov., sp. nov., a novel, extremely halophilic member of the Bacteria from saltern crystallizer ponds. Int J Syst Evol Microbiol 2002; 52:485–491 [View Article] [PubMed]
     [Google Scholar]
  58. Li Y, Sommerfeld M, Chen F, Hu Q. Consumption of oxygen by astaxanthin biosynthesis: A protective mechanism against oxidative stress in Haematococcus pluvialis (Chlorophyceae. J Plant Physiol 2008; 165:1783–1797 [View Article] [PubMed]
     [Google Scholar]
  59. Sanchez S, Ruiz B, Rodríguez-Sanoja R, Flores-Cotera LB. Microbial production of carotenoids. In Microbial Production of Food Ingredients, Enzymes and Nutraceuticals Elsevier; 2013 pp 194–233
     [Google Scholar]
  60. Nishino A, Maoka T, Yasui H. Analysis of reaction products of astaxanthin and its acetate with reactive oxygen species using LC/PDA ESI-MS and ESR spectrometry. Tetrahedron Lett 2016; 57:1967–1970 [View Article]
     [Google Scholar]
  61. McBride MJ, Zhu Y. Gliding motility and por secretion system genes are widespread among members of the phylum Bacteroidetes. J Bacteriol 2013; 195:270–278 [View Article] [PubMed]
     [Google Scholar]
  62. Wong SK, Park S, Lee J-S, Chul Lee K, Xavier Chiura H et al. Fabibacter misakiensis sp. nov., a marine bacterium isolated from coastal surface water. Int J Syst Evol Microbiol 2015; 65:3276–3280 [View Article] [PubMed]
     [Google Scholar]
  63. Nedashkovskaya OI, Kim SB, Shin DS, Beleneva IA, Mikhailov VV. Fulvivirga Kasyanovii gen. nov., sp. nov., a novel member of the phylum Bacteroidetes isolated from seawater in a mussel farm. Int J Syst Evol Microbiol 2007; 57:1046–1049 [View Article] [PubMed]
     [Google Scholar]
  64. Selvaratnam C, Thevarajoo S, Goh KM, Chan KG, Chong CS. Proposal to reclassify Roseivirga ehrenbergii (Nedashkovskaya et al., 2008) as Roseivirga seohaensis comb. nov., description of Roseivirga seohaensis subsp. aquiponti subsp. nov. and emendation of the genus Roseivirga. Int J Syst Evol Microbiol 2016; 66:5537–5543 [View Article] [PubMed]
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/ijsem/10.1099/ijsem.0.004866
Loading
Mangrovivirga cuniculi gen. nov., sp. nov., a moderately halophilic bacterium isolated from bioturbated Red Sea mangrove sediment, and proposal of the novel family Mangrovivirgaceae fam. nov.
Int J Syst Evol Microbiol 71, 004866 (2021); https://doi.org/10.1099/ijsem.0.004866
/content/journal/ijsem/10.1099/ijsem.0.004866
/content/journal/ijsem/10.1099/ijsem.0.004866
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF

Most cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error