Abstract
The genus Halioglobus is one of the environmentally relevant members of the family Halieaceae, class Gammaproteobacteria. At present, the genus is composed of three validly published species. However, in the recent study of the family Halieaceae, the species Halioglobus pacificus was observed to branch outside of the main clade formed by the members of Halioglobus, suggesting its distinct taxonomic placement within the family. In the present study, the taxonomic placement of H. pacificus was reassessed using comparative genomics. Phylogenomic analysis revealed the paraphyletic relationship of H. pacificus with the type species of the genus Halioglobus, and further demonstrated its genus-level placement. This phylogenetic relationship was reinforced by the average nucleotide and amino acid identity values shared by H. pacificus with the members of the family Halieaceae. Moreover, the results of the pan-genome analysis, together with the phenotype data, further supported the exclusion of H. pacificus from the genus Halioglobus. Based on these findings, the species H. pacificus is thereby assigned to a new genus Parahalioglobus gen. nov. as Parahalioglobus pacificus comb. nov.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
All data generated or analyzed in this study are included in this article and its supporting information.
References
Carpi FM, Coman MM, Silvi S et al (2022) Comprehensive pan-genome analysis of Lactiplantibacillus plantarum complete genomes. J Appl Microbiol 132:592–604. https://doi.org/10.1111/JAM.15199
Cho JC, Giovannoni SJ (2004) Cultivation and growth characteristics of a diverse group of oligotrophic marine Gammaproteobacteria. Appl Environ Microbiol 70:432–440. https://doi.org/10.1128/AEM.70.1.432-440.2004/ASSET/A3019E6D-E600-47EC-ABED-85313E548E89/ASSETS/GRAPHIC/ZAM0010411420004.JPEG
Chun J, Oren A, Ventosa A et al (2018) Proposed minimal standards for the use of genome data for the taxonomy of prokaryotes. Int J Syst Evol Microbiol 68:461–466. https://doi.org/10.1099/IJSEM.0.002516
Dereeper A, Summo M, Meyer DF (2022) PanExplorer: a web-based tool for exploratory analysis and visualization of bacterial pan-genomes. Bioinformatics 38:4412–4414. https://doi.org/10.1093/BIOINFORMATICS/BTAC504
Emms DM, Kelly S (2019) OrthoFinder: phylogenetic orthology inference for comparative genomics. Genome Biol 20:. https://doi.org/10.1186/S13059-019-1832-Y
Fuchs BM, Spring S, Teeling H et al (2007) Characterization of a marine gammaproteobacterium capable of aerobic anoxygenic photosynthesis. Proc Natl Acad Sci U S A 104:2891–2896. https://doi.org/10.1073/PNAS.0608046104/SUPPL_FILE/08046TABLE3.PDF
Han JR, Ye MQ, Wang C, Du ZJ (2019) Halioglobus sediminis sp. nov., isolated from coastal sediment. Int J Syst Evol Microbiol 69:1601–1605. https://doi.org/10.1099/IJSEM.0.003366/CITE/REFWORKS
Kanehisa M, Sato Y (2020) KEGG Mapper for inferring cellular functions from protein sequences. Protein Sci 29:28–35. https://doi.org/10.1002/PRO.3711
Kanehisa M, Sato Y, Morishima K (2016) BlastKOALA and GhostKOALA: KEGG tools for functional characterization of genome and metagenome sequences. J Mol Biol 428:726–731. https://doi.org/10.1016/J.JMB.2015.11.006
Kang JW, Yang HG, Choi S et al (2020) Seongchinamella unica gen. Nov., sp. nov., isolated from a tidal mudflat of beach, and transfer of Halioglobus sediminis to Seongchinamella sediminis comb. nov. and Halioglobus lutimaris to Pseudohalioglobus gen. nov. as Pseudohalioglobus lutimaris comb. nov. Int J Syst Evol Microbiol 70:2194–2203. https://doi.org/10.1099/IJSEM.0.003914/CITE/REFWORKS
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
Kuzmanović N, Fagorzi C, Mengoni A, et al (2022) Taxonomy of Rhizobiaceae revisited: proposal of a new framework for genus delimitation. Int J Syst Evol Microbiol 72:. https://doi.org/10.1099/IJSEM.0.005243
Letunic I, Bork P (2021) Interactive Tree Of Life (iTOL) v5: an online tool for phylogenetic tree display and annotation. Nucleic Acids Res 49:W293–W296. https://doi.org/10.1093/NAR/GKAB301
Li S-H, Kang I, Cho J-C (2023) Metabolic versatility of the family Halieaceae revealed by the genomics of novel cultured isolates . Microbiol Spectr 11:. https://doi.org/10.1128/SPECTRUM.03879-22/SUPPL_FILE/SPECTRUM.03879-22-S0001.PDF
Li SH, Song J, Lim Y et al (2020) Halioglobus maricola sp. nov., isolated from coastal seawater. Int J Syst Evol Microbiol 70:1868–1875. https://doi.org/10.1099/IJSEM.0.003985/CITE/REFWORKS
Mesa V, Monot M, Ferraris L et al (2022) Core-, pan- and accessory genome analyses of Clostridium neonatale: insights into genetic diversity. Microb Genom 8:000813. https://doi.org/10.1099/MGEN.0.000813/CITE/REFWORKS
Montecillo JA V. (2023) Phylogenomics and molecular marker-based analyses of the order Nevskiales: proposal for the creation of Steroidobacterales ord. nov. and Peristeroidobacter gen. nov. Res Microbiol 174:. https://doi.org/10.1016/J.RESMIC.2023.104057
Na SI, Kim YO, Yoon SH et al (2018) UBCG: up-to-date bacterial core gene set and pipeline for phylogenomic tree reconstruction. J Microbiol 56:281–285. https://doi.org/10.1007/S12275-018-8014-6
Park S, Yoshizawa S, Inomata K et al (2012) Halioglobus japonicus gen. nov., sp. nov. and halioglobus pacificus sp. nov., members of the class gammaproteobacteria isolated from seawater. Int J Syst Evol Microbiol 62:1784–1789. https://doi.org/10.1099/IJS.0.031443-0/CITE/REFWORKS
Parks DH, Chuvochina M, Rinke C et al (2022) GTDB: an ongoing census of bacterial and archaeal diversity through a phylogenetically consistent, rank normalized and complete genome-based taxonomy. Nucleic Acids Res 50:D785–D794. https://doi.org/10.1093/NAR/GKAB776
Parks DH, Chuvochina M, Waite DW, et al (2018) A standardized bacterial taxonomy based on genome phylogeny substantially revises the tree of life. Nature Biotechnology 36:10 36:996–1004. https://doi.org/10.1038/nbt.4229
Parks DH, Imelfort M, Skennerton CT et al (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
Parte AC, Carbasse JS, Meier-Kolthoff JP et al (2020) List of prokaryotic names with standing in nomenclature (LPSN) moves to the DSMZ. Int J Syst Evol Microbiol 70:5607–5612. https://doi.org/10.1099/IJSEM.0.004332/CITE/REFWORKS
Rajput A, Chauhan SM, Mohite OS et al (2023) Pangenome analysis reveals the genetic basis for taxonomic classification of the Lactobacillaceae family. Food Microbiol 115:104334. https://doi.org/10.1016/J.FM.2023.104334
Shi MJ, Wang C, Wang XT, Du ZJ (2018) Halioglobus lutimaris sp. nov., isolated from coastal sediment. Int J Syst Evol Microbiol 68:876–880. https://doi.org/10.1099/IJSEM.0.002601/CITE/REFWORKS
Spring S, Scheuner C, Göker M, Klenk HP (2015) A taxonomic framework for emerging groups of ecologically important marine gammaproteobacteria based on the reconstruction of evolutionary relationships using genome-scale data. Front Microbiol 6:134734. https://doi.org/10.3389/FMICB.2015.00281/ABSTRACT
Tang D, Chen M, Huang X et al (2023) SRplot: a free online platform for data visualization and graphing. PLoS ONE 18:e0294236. https://doi.org/10.1371/JOURNAL.PONE.0294236
Trojan D, Garcia-Robledo E, Meier D V., et al (2021) Microaerobic lifestyle at nanomolar O 2 concentrations mediated by low-affinity terminal oxidases in abundant soil bacteria . mSystems 6:. https://doi.org/10.1128/MSYSTEMS.00250-21/SUPPL_FILE/MSYSTEMS.00250-21-ST004.DOCX
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
Yan S, Fuchs BM, Lenk S et al (2009) Biogeography and phylogeny of the NOR5/OM60 clade of Gammaproteobacteria. Syst Appl Microbiol 32:124–139. https://doi.org/10.1016/J.SYAPM.2008.12.001
Yoon SH, Smin Ha, Lim J et al (2017) A large-scale evaluation of algorithms to calculate average nucleotide identity. Antonie Van Leeuwenhoek 110:1281–1286. https://doi.org/10.1007/S10482-017-0844-4
Zhang YN, Zhang TS, Chen XY et al (2022) Pseudohalioglobus sediminis sp. nov., isolated from coastal sediment. Arch Microbiol 204:1–7. https://doi.org/10.1007/S00203-022-02816-X/METRICS
Zheng J, Wittouck S, Salvetti E et al (2020) A taxonomic note on the genus Lactobacillus: description of 23 novel genera, emended description of the genus Lactobacillus Beijerinck 1901, and union of Lactobacillaceae and Leuconostocaceae. Int J Syst Evol Microbiol 70:2782–2858. https://doi.org/10.1099/IJSEM.0.004107
Zhu Q, Mai U, Pfeiffer W, et al (2019) Phylogenomics of 10,575 genomes reveals evolutionary proximity between domains Bacteria and Archaea. Nature Communications 2019 10:1 10:1–14. https://doi.org/10.1038/s41467-019-13443-4
Author information
Authors and Affiliations
Contributions
JAVM conceptualized the study, performed all the analyses, and wrote the manuscript.
Corresponding author
Ethics declarations
Ethical statement
No experiments with humans or animals were carried out.
Competing interests
The author declares no competing interests.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
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.
About this article
Cite this article
Montecillo, J.A.V. Comparative genomics of the genus Halioglobus reveals the genetic basis for the reclassification of Halioglobus pacificus as Parahalioglobus pacificus gen. nov. comb. nov. Int Microbiol (2024). https://doi.org/10.1007/s10123-024-00516-8
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s10123-024-00516-8