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Parendozoicomonas callyspongiae sp. nov. Isolated from a Marine Sponge, Callyspongia elongate, and Reclassification of Sansalvadorimonas verongulae as Parendozoicomonas verongulae comb. nov.

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Abstract

A strictly aerobic Gram-negative bacterium, designated 2012CJ34-2T, was isolated from marine sponge to Chuja-do in Jeju-island, Republic of Korea and taxonomically characterized. Cells were catalase- and oxidase-positive, and non-motile rods (without flagella). Growth was observed at 15–42 °C (optimum, 30 °C), pH 6–9 (optimum, pH 7), and in the presence of 0.5–10% (w/v) NaCl (optimum, 2–3%). The major cellular fatty acid and respiratory quinones were identified summed feature 3 (C16:1 ω7c/C16:1 ω6c), and Q-8 and Q-9, respectively. The polar lipids comprised diphosphatidylglycerol, phosphatidylglycerol, phosphatidylethanolamine, an unidentified aminophospholipid, two unidentified phospholipids, and three unidentified lipids. The DNA G+C content was 48.0 mol%. Phylogenetic analyses based on 16S rRNA gene and whole genome sequences showed that strain 2012CJ34-2T formed a clade with Parendozoicomonas haliclonae S-B4-1UT and Sansalvadorimonas verongulae LMG 29871T within the family Endozoicomodaceae. Genome relatedness values, including dDDH, ANI and AF, and AAI and POCP, among strain 2012CJ34-2T, P. haliclonae S-B4-1UT, and S. verongulae LMG 29871T were within the range of the bacterial genus cut-off values. Based on the phylogenetic, chemotaxonomic, and genomic analyses, strain 2012CJ34-2T represents a novel bacterial species of the family Endozoicomodaceae, for which the name Parendozoicomonas callyspongiae sp. nov. is proposed. The type strain is 2012CJ34-2T (= KACC 22641T = LMG 32581T). Additionally, we proposed the reclassification of Sansalvadorimonas verongulae of the family Hahellaceae as Parendozoicomonas verongulae of the family Endozoicomonadaceae.

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Fig. 1
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Abbreviations

ML:

Maximum-likelihood

NJ:

Neighbor-joining

MP:

Maximum-parsimony

Q:

Ubiquinone

ANI:

Average nucleotide identity

dDDH:

Digital DNA–DNA hybridization

AAI:

Average amino acid identity

POCP:

Percentage of conserved proteins

AF:

Alignment fraction

MA:

Marine agar

MB:

Marine broth

References

  1. Bartz JO, Blom J, Busse HJ, Mvie JB, Hardt M, Schubert P et al (2018) Parendozoicomonas haliclonae gen. nov., sp. nov., isolated from a marine sponge of the genus Haliclona and description of the family Endozoicomonadaceae fam. nov., comprising the genera Endozoicomonas, Parendozoicomonas, and Kistimonas. Syst Appl Microbiol 41:73–84. https://doi.org/10.1016/j.syapm.2017.11.004

    Article  PubMed  Google Scholar 

  2. Kurahashi M, Yokota A (2007) Endozoicomonas elysicola gen. nov., sp. nov., a γ-proteobacterium isolated from the sea slug Elysia ornata. Syst Appl Microbiol 30:202–206. https://doi.org/10.1016/j.syapm.2006.07.003

    Article  PubMed  CAS  Google Scholar 

  3. Yang CS, Chen MH, Arun AB, Chen CA, Wang JT (2010) Endozoicomonas montiporae sp. nov., isolated from the encrusting pore coral Montipora aequituberculata. Int J Syst Evol Microbiol 60:1158–1162. https://doi.org/10.1099/ijs.0.014357-0

    Article  PubMed  CAS  Google Scholar 

  4. Pike RE, Haltli B, Kerr RG (2013) Description of Endozoicomonas euniceicola sp. nov., and Endozoicomonas gorgoniicola sp. nov., bacteria isolated from the octocorals Eunicea fusca and Plexaura sp., and an emended description of the genus Endozoicomonas. Int J Syst Evol Microbiol 63:4294–4302. https://doi.org/10.1099/ijs.0.051490-0

    Article  PubMed  CAS  Google Scholar 

  5. Sheu SY, Lin KR, Hsu MY, Sheu DS, Tang SL (2017) Endozoicomonas acroporae sp. nov., isolated from Acropora coral. Int J Syst Evol Microbiol 67:3791–3797. https://doi.org/10.1099/ijsem.0.002194

    Article  PubMed  CAS  Google Scholar 

  6. Nishijima M, Adachi K, Katsuta A, Shizuri Y, Yamasato K (2013) Endozoicomonas numazuensis sp. nov., a gammaproteobacterium isolated from marine sponges, and emended description of the genus Endozoicomonas. Kurahashi and Yokota 2007. Int J Syst Evol Microbiol 63:709–714. https://doi.org/10.1099/ijs.0.042077-0

    Article  PubMed  CAS  Google Scholar 

  7. Hyun DW, Shin NR, Kim MS, Oh SJ, Kim PS (2014) Endozoicomonas atrinae sp. nov., isolated from the intestine of a comb pen shell Atrina pectinata. Int J Syst Evol Microbiol 64:2312–2318. https://doi.org/10.1099/ijs.0.060780-0

    Article  PubMed  CAS  Google Scholar 

  8. Appolinario LR, Tschoeke DA, Rua CP, Venas T, Campeão ME, Amaral GR et al (2016) Description of Endozoicomonas arenosclerae sp. nov., using a genomic taxonomy approach. Antonie Van Leeuwenhoek 109:431–438. https://doi.org/10.1007/s10482-016-0649-x

    Article  PubMed  Google Scholar 

  9. Schreiber L, Kjeldsen KU, Obst M, Funch P, Schramm A (2016) Description of Endozoicomonas ascidiicola sp. nov., isolated from Scandinavian ascidians. Syst Appl Microbiol 39:313–318. https://doi.org/10.1016/j.syapm.2016.05.008

    Article  PubMed  CAS  Google Scholar 

  10. Choi EJ, Kwon HC, Sohn YC, Yang HO (2010) Kistimonas asteriae gen. nov., sp. nov., a gammaproteobacterium isolated from Asterias amurensis. Int J Syst Evol Microbiol 60:938–943. https://doi.org/10.1099/ijs.0.014282-0

    Article  PubMed  CAS  Google Scholar 

  11. Lee J, Shin NR, Lee HW, Roh SW, Kim MS, Kim YO et al (2012) Kistimonas scapharcae sp. nov., isolated from a dead ark clam (Scapharca broughtonii), and emended description of the genus Kistimonas. Int J Syst Evol Microbiol 62:2865–2869. https://doi.org/10.1099/ijs.0.038422-0

    Article  PubMed  CAS  Google Scholar 

  12. Taylor MW, Radax R, Steger D, Wagner M (2007) Sponge-associated microorganisms: evolution, ecology, and biotechnological potential. Microbiol Mol Biol Rev 71:295–347. https://doi.org/10.1128/mmbr.00040-06

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  13. Schmitt S, Tsai P, Bell J, Fromont J, Ilan M, Lindquist N et al (2012) Assessing the complex sponge microbiota: core, variable and species-specific bacterial communities in marine sponges. ISME J 6:564–576. https://doi.org/10.1038/ismej.2011.116

    Article  PubMed  CAS  Google Scholar 

  14. Taylor MW, Schupp PJ, de Nys R, Kjelleberg S, Steinberg PD (2005) Biogeography of bacteria associated with the marine sponge Cymbastela concentrica. Environ Microbiol 7:419–433. https://doi.org/10.1111/j.1462-2920.2004.00711.x

    Article  PubMed  CAS  Google Scholar 

  15. Storey MA, Andreassend SK, Bracegirdle J, Brown A, Keyzers RA, Ackerley DF et al (2020) Metagenomic exploration of the marine sponge Mycale hentscheli uncovers multiple polyketide-producing bacterial symbionts. MBio 11:1110–1128. https://doi.org/10.1128/mbio.02997-19

    Article  CAS  Google Scholar 

  16. 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  PubMed  PubMed Central  CAS  Google Scholar 

  17. Lane DJ (1991) 16S/23S rRNA sequencing. In: Stackebrandt E, Goodfellow M (eds) Nucleic acid techniques in bacterial systematic. Wiley, New York, pp 115–175

    Google Scholar 

  18. Yoon SH, Ha SM, Kwon S, Lim J, Kim Y (2017) Introducing EzBioCloud: a taxonomically united database of 16S rRNA and whole genome assemblies. Int J Syst Evol Microbiol 67:1613–1617. https://doi.org/10.1099/ijsem.0.001755

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  19. Nawrocki EP, Eddy SR (2013) Infernal 1.1: 100-fold faster RNA homology searches. Bioinformatics 29:2933–2935. https://doi.org/10.1093/bioinformatics/btt509

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  20. Tamura K, Stecher G, Kumar S (2021) MEGA11: molecular evolutionary genetics analysis version 11. Mol Biol Evol 38:3022–3027. https://doi.org/10.1093/molbev/msab120

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  21. Li R (2010) De novo assembly of human genomes with massively parallel short read sequencing. Genome Res 20:265–272. https://doi.org/10.1101/gr.097261.109

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  22. 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. https://doi.org/10.1101/gr.186072.114

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  23. Tatusova T, DiCuccio M, Badretdin A, Chetvernin V, Nawrocki EP (2016) NCBI prokaryotic genome annotation pipeline. Nucleic Acids Res 44:6614–6624. https://doi.org/10.1093/nar/gkw569

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  24. Kim J, Na SI, Kim D, Chun J (2021) UBCG2: up-to-date bacterial core genes and pipeline for phylogenomic analysis. J Microbiol 59:609–615. https://doi.org/10.1007/s12275-021-1231-4

    Article  PubMed  CAS  Google Scholar 

  25. Yoon SH, Ha SM, Lim J, Kwon S, Chun J (2017) A largescale evaluation of algorithms to calculate average nucleotide identity. Antonie Van Leeuwenhoek 110:1281–1286. https://doi.org/10.1007/s10482-017-0844-4

    Article  PubMed  CAS  Google Scholar 

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

    Article  Google Scholar 

  27. Konstantinidis KT, Tiedje JM (2005) Towards a genome-based taxonomy for prokaryotes. J Bacteriol 187:6258–6264. https://doi.org/10.1128/JB.187.18.6258-6264.2005

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  28. Kim D, Park S, Chun J (2021) Introducing EzAAI: a pipeline for high throughput calculations of prokaryotic average amino acid identity. J Microbiol 59:476–480. https://doi.org/10.1007/s12275-021-1154-0

    Article  PubMed  CAS  Google Scholar 

  29. Qin QL, Xie BB, Zhang XY, Chen XL, Zhou BC, Zhou J et al (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  CAS  Google Scholar 

  30. Zheng J, Ge Q, Yan Y, Zhang X, Huang L, Yin Y (2023) dbCAN3: automated carbohydrate-active enzyme and substrate annotation. Nucleic Acids Res 51:W115–W121. https://doi.org/10.1093/nar/gkad328

    Article  PubMed  PubMed Central  Google Scholar 

  31. Perry LB (1973) Gliding motility in some non-spreading flexibacteria. J Appl Bacteriol 36:227–232. https://doi.org/10.1111/j.1365-2672.1973.tb04095.x

    Article  PubMed  CAS  Google Scholar 

  32. Buck JD (1982) Nonstaining (KOH) method for determination of Gram reactions of marine bacteria. Appl Environ Microbiol 44:992–993. https://doi.org/10.1128/aem.44.4.992-993.1982

    Article  PubMed  PubMed Central  ADS  CAS  Google Scholar 

  33. Smibert RM, Krieg NR (1994) Phenotypic characterization. In: Gerhardt P (ed) Methods for general and molecular bacteriology. American Society for Microbiology, Washington, pp 607–654

    Google Scholar 

  34. Weon HY, Kim BY, Joa JH, Son JA, Song MH (2008) Methylobacterium iners sp. nov. and Methylobacterium aerolatum sp. nov., isolated from air samples in Korea. Int J Syst Evol Microbiol 58:93–96. https://doi.org/10.1099/ijs.0.65047-0

    Article  PubMed  CAS  Google Scholar 

  35. Lanyi B (1988) Classical and rapid identification methods for medically important bacteria. In: Colwell RR, Grigorova R (eds) Methods in microbiology, vol 19. Elsevier, New York, pp 1–67

    Google Scholar 

  36. Minnikin DE, O’Donnell AG, Goodfellow M, Alderson G, Athalye M (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 

  37. Hiraishi A, Ueda Y, Ishihara J, Mori T (1996) Comparative lipoquinone analysis of influent sewage and activated sludge by high-performance liquid chromatography and photodiode array detection. J Gen Appl Microbiol 42:457–469. https://doi.org/10.2323/jgam.42.457

    Article  CAS  Google Scholar 

  38. Sasser M (1990) Identification of bacteria by gas chromatography of cellular fatty acids. MIDI Technical Note 101

  39. Volpiano CG, Sant’Anna FH, da Mota FF, Sangal V, Sutcliffe I, Munusamy M et al (2021) Proposal of Carbonactinosporaceae fam. Nov. within the class Actinomycetia. Reclassification of Streptomyces thermoautotrophicus as Carbonactinospora thermoautotrophica gen. nov., comb. Nov. Syst Appl Microbiol 44:126223. https://doi.org/10.1016/j.syapm.2021.126223

    Article  PubMed  CAS  Google Scholar 

  40. Kumar S, Bansal K, Patil PP, Patil PB (2019) Phylogenomics insights into order and families of Lysobacterales. Access Microbiol 1:e000015. https://doi.org/10.1099/acmi.0.000015

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  41. Park MJ, Kim YJ, Park M, Yu J, Namirimu T, Roh YR et al (2022) Establishment of genome based criteria for classification of the family Desulfovibrionaceae and proposal of two novel genera, Alkalidesulfovibrio gen. nov. and Salidesulfovibrio gen. nov. Front Microbiol 13:738205. https://doi.org/10.3389/fmicb.2022.738205

    Article  PubMed  PubMed Central  Google Scholar 

  42. Barco RA, Garrity GM, Scott JJ, Amend JP, Nealson KH et al (2020) A genus definition for bacteria and archaea based on a standard genome relatedness index. MBio 11:e02475-e2519. https://doi.org/10.1128/mBio.02475-19

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  43. Pita L, Rix L, Slaby BM, Franke A, Hentschel U (2018) The sponge holobiont in a changing ocean: from microbes to ecosystems. Microbiome 6:1–18. https://doi.org/10.1186/s40168-018-0428-1

    Article  Google Scholar 

  44. Goldberg SR, Haltli BA, Correa H, Kerr RG (2018) Description of Sansalvadorimonas verongulae gen. nov., sp. nov., a gammaproteobacterium isolated from the marine sponge Verongula gigantea. Int J Syst Evol Microbiol 68:2006–2014. https://doi.org/10.1099/ijsem.0.002781

    Article  PubMed  CAS  Google Scholar 

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Acknowledgements

This research was supported by the management of Marine Fishery Bio-resources Center (2023) funded by the National Marine Biodiversity Institute of Korea (MABIK), and Basic Science Research Program through the National Research Foundation of Korea (NRF) funded by the Ministry of Education (2021R1I1A3046479). We gratefully thank Professor (Emeritus) Aharon Oren, The Hebrew University of Jerusalem, for reviewing nomenclature for new names of bacterial species.

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JSP conceived the ideas and supervised all works. SBK collected the samples, isolated the strain, and performed initial cultivation, storage, and deposition, and sequenced and analyzed the genome. SBK and KHK analyzed the phenotypic, biochemical, and genomic properties. SBK and JSP wrote the manuscript, and the manuscript has been reviewed and edited by all authors.

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Correspondence to Jin-Sook Park.

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The GenBank accession number for the 16S rRNA gene and whole genome sequences of strain 2012CJ34-2T are OM647832 and JAMFLX000000000, respectively.

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Kim, SB., Kim, K.H. & Park, JS. Parendozoicomonas callyspongiae sp. nov. Isolated from a Marine Sponge, Callyspongia elongate, and Reclassification of Sansalvadorimonas verongulae as Parendozoicomonas verongulae comb. nov.. Curr Microbiol 81, 85 (2024). https://doi.org/10.1007/s00284-023-03585-6

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