Abstract
A novel Gram-staining negative, strictly aerobic, rod-shaped, and non-motile bacterium, designated strain 9Alg 56T, was isolated from the red alga Tichocarpus crinitus. The phylogenetic analysis based on 16S rRNA gene sequences placed the novel strain within the family Rhodobacteraceae, the order Rhodobacterales, the class Alphaproteobacteria, the phylum Pseudomonadota. The nearest neighbors of the new strain were Pontivivens insulae KCTC 42458T, Oceanibium sediminis KCTC 62076T, Halovulum dunhuangense YYQ-30T and Monaibacterium marinum C7T with 16S rRNA gene sequence similarity of 94.7, 94.4%, 93.1 and 92.7%, respectively. The AAI/ANI/dDDH values between 9Alg 56T and the five species of the closest genera (Pontivivens, Oceanibium, Halovulum, Monaibacterium, and ‘Oceanomicrobium’) were 58.63–63.91%/ 75.91–77.37%/ 19.3–20.4%. The prevalent fatty acids of strain 9Alg 56T were C18:1 ω7c, C18:0 and C14:0 3-OH. The polar lipid profile consisted of phosphatidylethanolamine, phosphatidylglycerol, phosphatidic acid, phosphatidylcholine, and two unidentified lipids. The DNA G+C content of strain 9Alg 56T was 61.5 mol%. A combination of the genotypic and phenotypic data showed that the algal isolate represents a novel genus and species, for which the name Algicella marina gen. nov., sp. nov. is proposed. The type strain is 9Alg 56T (= KCTC 72005T = KMM 6775T).
Similar content being viewed by others
References
Asnicar F, Thomas AM, Beghini F, Mengoni C, Manara S, Manghi P, Zhu Q, Bolzan M, Cumbo F, May U, Sanders JG, Zolfo M, Kopylova E, Pasolli E, Knight R, Mirarab S, Huttenhower C, Sanders JG (2020) Precise phylogenetic analysis of microbial isolates and genomes from metagenomes using PhyloPhlAn 3.0. Nat Commun 11:1–10. https://doi.org/10.1038/s41467-020-16366-7
Chang YQ, Men X, Du ZZ, Du ZJ (2019) Oceanibium sediminis gen. nov., sp. nov., isolated from marine sediment. Int J Syst Evol Microbiol 69:249–254. https://doi.org/10.1099/ijsem.0.003139
Chernikova TN, Dallimore J, Lünsdorf H, Heipieper HJ, Golyshin PN (2017) Monaibacterium marinum, gen. nov, sp. nov, a new member of the Alphaproteobacteria isolated from seawater of Menai Straits, Wales, UK. Int J Syst Evol Microbiol 67:3310–3317. https://doi.org/10.1099/ijsem.0.002111
Chin CS, Alexander DH, Marks P, Klammer AA, Drake J, Heiner C, Clum A, Copeland A, Huddleston J, Eichler EE, Turner SW, Korlach J (2013) Nonhybrid, finished microbial genome assemblies from long-read SMRT sequencing data. Nat Methods 10(6):563–569
Colston SM, Fullmer MS, Beka L, Lamy B, Gogarten JP, Graf J (2014) Bioinformatic genome comparisons for taxonomic and phylogenetic assignments using Aeromonas as a test case. mBio 5(6):e02136. https://doi.org/10.1128/mBio.02136-14
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
Felsenstein J (1993) PHYLIP (phylogenetic inference package), version 3.5c. Department of Genetic, University of Washington, Seattle, USA
Feng T, Kim KH, Jeong SE, Kim W, Jeon CO (2018) Aquicoccus porphyridii gen. nov., sp. nov., isolated from a small marine red alga, Porphyridium marinum. Int J Syst Evol Microbiol 68:283–288. https://doi.org/10.1099/ijsem.0.002498
Fukui Y, Abe M, Kobayashi M, Ishihara K, Oikawa H, Yano Y, Satomi M (2012) Maritalea porphyrae sp. nov., isolated from a red alga (Porphyra yezoensis), and transfer of Zhangella mobilis to Maritalea mobilis comb. nov. Int J Syst Evol Microbiol 62:43–48. https://doi.org/10.1099/ijs.0.028704-0
Fukui Y, Abe M, Kobayashi M, Saito H, Oikawa H, Yano Y, Satomi M (2013a) Algimonas porphyrae gen. nov., sp. nov., a member of the family Hyphomonadaceae, isolated from the red alga Porphyra yezoensis. Int J Syst Evol Microbiol 63:314–320. https://doi.org/10.1099/ijs.0.040485-0
Fukui Y, Kobayashi M, Saito H, Oikawa H, Yano Y, Satomi M (2013b) Algimonas ampicilliniresistens sp. nov., isolated from the red alga Porphyra yezoensis, and emended description of the genus Algimonas. Int J Syst Evol Microbiol 63:4407–4412. https://doi.org/10.1099/ijs.0.053405-0
Fukui Y, Abe M, Kobayashi M, Shimada Y, Saito H, Oikawa H, Yano Y, Satomi M (2014) Sulfitobacter porphyrae sp. nov., isolated from the red alga Porphyra yezoensis. Int J Syst Evol Microbiol 64:438–443. https://doi.org/10.1099/ijs.0.053090-0
Gerhardt P, Murray RGE, Wood WA, Krieg NR (Eds) (1994) Methods for general and molecular bacteriology. American Society for Microbiology, Washington, DC
Huerta-Cepas J, Szklarczyk D, Heller D, Hernández-Plaza A, Forslund SK, Cook H, Mende DR, Letunic I, Rattei T, Jensen LJ, von Mering C, Bork P (2019) eggNOG 5.0: a hierarchical, functionally and phylogenetically annotated orthology resource based on 5090 organisms and 2502 viruses. Nucleic Acids Res 47(D1): D309–D314. https://doi.org/10.1093/nar/gky1085
Jeong SE, Kim KH, Lhee D, Yoon HS, Quan ZX, En-Y L, Jeon CO (2019) Oceaniradius stylonematis gen. nov., sp. nov., isolated from a red alga, Stylonema cornu-cervi. Int J Syst Evol Microbiol 69:1967–1973. https://doi.org/10.1099/ijsem.0.003413
Jeong SE, Kim KH, Baek K, Jeon CO (2017) Parasphingopyxis algicola sp. nov., isolated from a marine red alga Asparagopsis taxiformis and emended description of the genus Parasphingopyxis Uchida et al. Int J Syst Evol Microbiol 67:3877–3881. https://doi.org/10.1099/ijsem.0.002215
Jung HS, Jeong SE, Chun BH, Quan ZX, Jeon CO (2019) Rhodophyticola porphyridii gen. nov., sp. nov., isolated from a red alga, Porphyridium marinum. Int J Syst Evol Microbiol 69:1656–1661. https://doi.org/10.1099/ijsem.0.003371
Kalyaanamoorthy S, Minh BQ, Wong TKF, von Haeseler A, Jermiin LS (2017) Modelfinder: Fast model selection for accurate phylogenetic estimates. Nat Methods 14:587–589
Kim J, Jeong SE, Khan SA, Jeon CO (2019) Hwanghaeella grinnelliae gen. nov., sp. nov., isolated from a marine red alga. Int J Syst Evol Microbiol 69(11):3544–3550. https://doi.org/10.1099/ijsem.0.003656
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
Kluge AG, Farris FS (1969) Quantitative phyletics and the evolution of anurans. Syst Zool 18:1–32. https://doi.org/10.1093/sysbio/18.1.1
Komagata K, Suzuki KI (1987) Lipid and cell wall analysis in bacterial systematics. Methods Microbiol 19:161–207. https://doi.org/10.1016/S0580-9517(08)70410-0
Kumar S, Stecher G, Tamura K (2016) MEGA7: Molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874. https://doi.org/10.1093/molbev/msw054
Lane DJ (1991) 16S/23S rRNA sequencing. In: Stackebrandt E, Goodfellow M (eds) Nucleic acid techniques in bacterial systematics. Wiley, Chichester, pp 115–175
Lemos ML, Toranzo AE, Barja JL (1985) Modifed medium for oxidation-fermentation test in the identification of marine bacteria. Appl Environ Microbiol 40:1541–1543. https://doi.org/10.1128/aem.49.6.1541-1543.1985
Luo C, Rodriguez-R LM, Konstantinidis KT (2014) MyTaxa: an advanced taxonomic classifier for genomic and metagenomic sequences. Nucleic Acids Res 42(8):e73. https://doi.org/10.1093/nar/gku169
Meier-Kolthof JP, Göker M (2019) TYGS is an automated high-throughput platform for state-of-the-art genome-based taxonomy. Nat Commun 1:1–10. https://doi.org/10.1038/s41467-019-10210-3
Miranda LN, Hutchison K, Grossman AR, Brawley SH (2013) Diversity and abundance of the bacterial community of the red macroalga Porphyra umbilicalis: did bacterial farmers produce macroalgae? PLoS ONE 8(3):e58269. https://doi.org/10.1371/journal.pone.0058269
Nedashkovskaya OI, Kim SB, Zhukova NV, Kwak J, Mikhailov VV, Bae KS (2006) Mesonia mobilis sp. nov., isolated from seawater, and emended description of the genus Mesonia. Int J Syst Evol Microbiol 56:2433–2436. https://doi.org/10.1099/ijs.0.64376-0
Park S, Won SM, Park JM, Jung YT, Yoon JH (2015) Pontivivens insulae gen. nov., sp. nov., isolated from seawater. Int J Syst Evol Microbiol 65:2896–2902. https://doi.org/10.1099/ijs.0.000352
Richter M, Rosselló-Móra R (2009) Shifting the genomic gold standard for the prokaryotic species definition. Proc Natl Acad Sci USA 06:19126–19131. https://doi.org/10.1073/pnas.0906412106
Rodriguez-R LM, Konstantinidis KT (2016) The enveomics collection: a toolbox for specialized analyses of microbial genomes and metagenomes. PeerJ. https://doi.org/10.7287/peerj.preprints.1900v1
Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Höhna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61(3):539–542. https://doi.org/10.1093/sysbio/sys029
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
Sambrook J, Russell DW (eds) (2001) Molecular cloning: a Laboratory Manual Cold Spring Harbor. Cold Spring Harbor Laboratory Press, New York
Smibert RM, Krieg NR (1994) Phenotypic characterization. In: Gerhardt P, Murray RGE, Wood WA, Krieg NR (eds) Methods for general and molecular bacteriology. American Society for Microbiology, Washington, pp 607–654
Sun F, Du Y, Liu X, Lai Q, Shao Z (2015) Halovulum dunhuangense gen. nov., sp. nov., isolated from a saline terrestrial spring. Int J Syst Evol Microbiol 65:2810–2816. https://doi.org/10.1099/ijs.0.000332
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 14:6614–6624. https://doi.org/10.1093/nar/gkw569
Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680. https://doi.org/10.1093/nar/22.22.4673
Wirth JS, Whitman WB (2018) Phylogenomic analyses of a clade within the roseobacter group suggest taxonomic reassignments of species of the genera Aestuariivita, Citreicella, Loktanella, Nautella, Pelagibaca, Ruegeria, Thalassobius, Thiobacimonas and Tropicibacter, and the proposal of six novel genera. Int J Syst Evol Microbiol 68:2393–2411. https://doi.org/10.1099/ijsem.0.002833
Yoon SH, Ha SM, Kwon S, Lim J, Kim Y, Seo H, Chun J (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
Funding
This research was funded by a grant from the Ministry of Science and Higher Education, Russian Federation 15.BRK.21.0004 (Contract No. 075-15-2021-1052).
Author information
Authors and Affiliations
Contributions
O.N., S-G.K. and M.I. planned the research and wrote the main manuscript text. O.N., S-G.K., A.K., and N.Z. carried out experiments. O.N., S-G.K., N.O., N.Z. and M.I. analysed the data and prepared figures. O.N. and M.I. supervised the research. All authors proofread the manuscript.
Corresponding authors
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
The whole genome sequence and 16S rRNA of Algicella marina gen. nov., sp. nov. strain 9Alg 56T have been deposited into GenBank/EMBL/DDBJ under accession numbers CP046620 and MN813959, respectively.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Nedashkovskaya, O.I., Otstavnykh, N.Y., Kim, SG. et al. Algicella marina gen. nov., sp. nov., a novel marine bacterium isolated from a Pacific red alga. Arch Microbiol 204, 487 (2022). https://doi.org/10.1007/s00203-022-03091-6
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00203-022-03091-6