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.
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
Sasser M (1990) Identification of bacteria by gas chromatography of cellular fatty acids. MIDI Technical Note 101
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
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
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
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
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
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
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.
Author information
Authors and Affiliations
Contributions
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.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no competing financial conflicts of interest.
Ethical Approval
The authors have declared that no ethical issues exist.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
The GenBank accession number for the 16S rRNA gene and whole genome sequences of strain 2012CJ34-2T are OM647832 and JAMFLX000000000, respectively.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
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
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00284-023-03585-6