Abstract
Phylogenomic analyses were performed on the nine species of the genus Meiothermus and four species of the genus Calidithermus. Phylogenetic analysis, low values of genomic relatedness indices and functional diversity analysis indicated that Meiothermus silvanus should not be classified within the clades for Meiothermus and Calidithermus but instead be reclassified as a new genus, for which we propose the name Allomeiothermus gen. nov., with Allomeiothermus silvanus comb. nov. as type species. In addition, the species Meiothermus cateniformans Zhang et al. (Int J Syst Evol Microbial 60:840–844, 2010) should also be reclassified as a later heterotypic synonym of Meiothermus taiwanensis Chen et al. (Int J Syst Evol Microbiol 52:1647–1654, 2002) emend. Raposo et al. (2019). This reclassification is based on the high genomic relatedness indices (98.8% ANI; 90.2% dDDH; 99% AAI) that are above the threshold values necessary for defining a new species, as well as on the observation of overlapping functions on Principal Coordinate Analysis plot generated from Clusters of Orthologous Genes.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
Three supplementary tables and six supplementary figures are included on the online supplementary files.
References
Albuquerque L, Rainey FA, da Costa MS (2018) Genus Meiothermus. In: Whitman WB et al (eds) Bergey’s Manual of Systematics of Archaea and Bacteria. Wiley, London, pp 1–28
Brock TD, Freeze H (1969) Thermus aquaticus gen. nov. and sp. nov., a nonsporulating extreme thermophile. J Bacteriol 98:289–297. https://doi.org/10.1128/jb.98.1.289-297.1969
Buchfink B, Xie C, Huson DH (2015) Fast and sensitive protein alignment using DIAMOND. Nat Methods 12:59–60. https://doi.org/10.1038/nmeth.3176
Chaumeil PA, Mussig AJ, Hugenholtz P, Parks DH (2019) GTDB-Tk: a toolkit to classify genomes with the genome taxonomy database. Bioinformatics 36:1925–1927. https://doi.org/10.1093/bioinformatics/btz848
Chen MY, Lin GH, Lin YT, Tsay SS (2002) Meiothermus taiwanensis sp. nov., a novel filamentous, thermophilic species isolated in Taiwan. Int J Syst Evol Microbiol 52:1647–1654. https://doi.org/10.1099/00207713-52-5-1647
Emms DM, Kelly S (2015) OrthoFinder: solving fundamental biases in whole genome comparisons dramatically improves orthogroup inference accuracy. Genome Biol 16:157. https://doi.org/10.1186/s13059-015-0721-2
Felsenstein J (1981) Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol 17:368–376. https://doi.org/10.1007/BF01734359
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
Fitch WM (1971) Toward defining the course of evolution: minimum change for a specific tree topology. Syst Zool 20:406–416. https://doi.org/10.1093/sysbio/20.4.406
Goris J, Konstantinidis KT, Klappenbach JA, Coenye T, Vandamme P, Tiedje JM (2007) DNA–DNA hybridization values and their relationship to whole-genome sequence similarities. Int J Syst Evol Microbiol 57:81–91. https://doi.org/10.1099/ijs.0.64483-0
Gupta RS (2019) Distinction between Borrelia and Borreliella is more robustly supported by molecular and phenotypic characteristics than all other neighbouring prokaryotic genera: response to Margos' et al." The genus Borrelia reloaded"(PLoS ONE 13 (12): e0208432). PLoS One 14:e0221397. doi: https://doi.org/10.1371/journal.pone.0221397
Hyatt D, Chen GL, Locascio PF, Land ML, Larimer FW, Hauser LJ (2010) Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC Bioinform 11:119. https://doi.org/10.1186/1471-2105-11-119
Jiao JY, Fu L, Hua ZS, Liu L, Salam N, Liu PF, Lv AP, Wu G, Xian WD, Zhu Q, Zhou EM, Fang BZ, Oren A, Hedlund BP, Jiang HC, Knight R, Cheng L, Li WJ (2021) Insight into the function and evolution of the Wood-Ljungdahl pathway in Actinobacteria. ISME J. https://doi.org/10.1038/s41396-021-00935-9
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. https://doi.org/10.1038/nmeth.4285
Kontantinidis KT, Tiedje JM (2007) Prokaryotic taxonomy and phylogeny in the genomic era: advancements and challenges ahead. Curr Opin Microbiol 10:504–509. https://doi.org/10.1016/j.mib.2007.08.006
Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35:1547–1549. https://doi.org/10.1093/molbev/msy096
Meier-Kolthoff JP, Auch AF, Klenk HP, Göker M (2013) Genome sequence-based species delimitation with confidence intervals and improved distance functions. BMC Bioinform 14:1–14. https://doi.org/10.1186/1471-2105-14-60
Moriya Y, Itoh M, Okuda S, Yoshizawa A, Kanehisa M (2007) KAAS: an automatic genome annotation and pathway reconstruction server. Nucleic Acids Res 35:182–185. https://doi.org/10.1093/nar/gkm321
Nguyen LT, Schmidt HA, von Haeseler A, Minh BQ (2014) IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol Biol Evol 32:268–274. https://doi.org/10.1093/molbev/msu300
Nicholson AC, Gulvik CA, Whitney AM, Humrighouse BW, Bell ME, Holmes B, Steigerwalt AG, Villarma A, Sheth M, Batra D, Rowe LA, Burroughs M, Pryor JC, Bernardet JF, Hugo C, Kämpfer P, Newman JD, McQuiston JR (2020) Division of the genus Chryseobacterium: observation of discontinuities in amino acid identity values, a possible consequence of major extinction events, guides transfer of nine species to the genus Epilithonimonas, eleven species to the genus Kaistella, and three species to the genus Halpernia gen. nov., with description of Kaistella daneshvariae sp. nov. and Epilithonimonas vandammei sp. nov. derived from clinical specimens. Int J Syst Evol Microbiol 70:4432–4450. https://doi.org/10.1099/ijsem.0.003935
Nobre MF, Truper HG, da Costa MS (1996) Transfer of Thermus ruber (Loginova et al. 1984), Thermus silvanus (Tenreiro et al. 1995), and Thermus chliarophilus (Tenreiro et al. 1995) to Meiothermus gen. nov. as Meiothermus ruber comb. nov., Meiothermus silvanus comb. nov., and Meiothermus chliarophilus comb. nov., respectively, and emendation of the genus Thermus. Int J Syst Evol Microbiol 46:604-606. doi: https://doi.org/10.1099/00207713-46-2-604
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
Parks DH, Chuvochina M, Rinke C, Mussig AJ, Chaumeil PA, Hugenholtz P (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
Parte AC, Carbasse JS, Meier-Kolthoff JP, Reimer LC, Göker M (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
Pritchard L, Glover RH, Humphris S, Elphinstone JG, Toth IK (2016) Genomics and taxonomy in diagnostics for food security: soft-rotting enterobacterial plant pathogens. Anal Methods 8:12–24. https://doi.org/10.1039/C5AY02550H
Qin QL, Xie BB, Zhang XY, Chen XL, Zhou BC, Zhou J, Oren A, Zhang YZ (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
Rafael R, Minegishi H, Kamekura M, Shimane Y, Ventosa A (2021) Phylogenomics of Haloarchaea: the controversy of the genera Natrinema-Haloterrigena. Front Microbiol 12:740909. https://doi.org/10.3389/fmicb.2021.740909
Raposo P, Viver T, Albuquerque L, Froufe H, Barroso C, Egas C, Rosselló-Móra R, da Costa MS (2019) Transfer of Meiothermus chliarophilus (Tenreiro et al.1995) Nobre et al. 1996, Meiothermus roseus Ming et al. 2016, Meiothermus terrae Yu et al. 2014 and Meiothermus timidus Pires et al. 2005, to Calidithermus gen. nov., as Calidithermus chliarophilus comb. nov., Calidithermus roseus comb. nov., Calidithermus terrae comb. nov. and Calidithermus timidus comb. nov., respectively, and emended description of the genus Meiothermus. Int J Syst Evol Microbiol 69:1060-1069. doi: https://doi.org/10.1099/ijsem.0.003270
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
Salam N, Jiao JY, Zhang XT, Li WJ (2020) Update on the classification of higher ranks in the phylum Actinobacteria. Int J Syst Evol Microbiol 70:1331–1355. https://doi.org/10.1099/ijsem.0.003920
Sikorski J, Tindall BJ, Lowry S, Lucas S, Nolan M, Copeland A, Del Rio TG, Tice H, Cheng JF, Han C, Pitluck S, Liolios K, Ivanova N, Mavromatis K, Mikhailova N, Pati A, Goodwin L, Chen A, Palaniappan K, Land M, Hauser L, Chang YJ, Jeffries CD, Rohde M, Göker M, Woyke T, Bristow J, Eisen JA, Markowitz V, Hugenholtz P, Kyrpides NC, Klenk HP, Lapidus A (2010) Complete genome sequence of Meiothermus silvanus type strain (VI-R2T). Stand Genom Sci 3:37–46. https://doi.org/10.4056/sigs.1042812
Tenreiro S, Nobre MF, da Costa MS (1995) Thermus silvanus sp. nov. and Thermus chliarophilus sp. nov., two new species related to Thermus ruber but with lower growth temperatures. Int J Syst Evol Microbiol 45:633–639. https://doi.org/10.1099/00207713-45-4-633
Wickham H (2011) ggplot2. Wiley Interdiscip Rev Comput Stat. 3.2 180-185
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
Xu Z, Masuda Y, Itoh H, Ushijima N, Shiratori Y, Senoo K (2019) Geomonas oryzae gen. nov., sp. nov., Geomonas edaphica sp. nov., Geomonas ferrireducens sp. nov., Geomonas terrae sp. nov., four ferric-reducing bacteria isolated from paddy soil, and reclassification of three species of the genus Geobacter as members of the genus Geomonas gen. nov. Front Microbiol 10: 2201. doi: https://doi.org/10.3389/fmicb.2019.02201
Xu Z, Masuda Y, Wang X, Ushijima N, Shiratori Y, Senoo K, Itoh H (2021) Genome-based taxonomic rearrangement of the order Geobacterales including the description of Geomonas azotofigens sp. Nov. and Geomonas diazotrophica sp. nov. Front Microbiol 12:737531. https://doi.org/10.3389/fmicb.2021.737531
Yoon SH, Ha SM, Kwon S, Lim J, Kim Y, Seo H, Chun J (2017) Introducing EzBioCloud: a taxonomically united database of 16S rRNA gene sequences and whole-genome assemblies. Int J Syst Evol Microbiol 67:1613–1617. https://doi.org/10.1099/ijsem.0.001755
Zhang XQ, Zhang WJ, Wei BP, Xu XW, Zhu XF, Wu M (2010) Meiothermus cateniformans sp. nov., a slightly thermophilic species from north-eastern China. Int J Syst Evol Microbiol 60:840–844. https://doi.org/10.1099/ijs.0.007914-0
Acknowledgements
The authors are grateful to Prof. Aharon Oren (The Hebrew University of Jerusalem, Israel) for helping with the etymology.
Funding
This study was supported by funding from National Natural Science Foundation of China (Nos. 91951205 and 31970122), Guangdong Provincial Construction Project of Agricultural Science and Technology Innovation and Extension System (2020KJ264), Guangdong Provincial Special Research Grant for the creation of National Parks (2021GJGY034) and Open project of Hebei Province Key Laboratory of Microbial Diversity Research and Application (MDRA202105). Wen-Jun Li was also supported by Introduction project of high-level talents in Xinjiang Uygur Autonomous Region.
Author information
Authors and Affiliations
Contributions
WJL and NS jointly conceived the study. Authors JYJ, ZHL, ZTL, LL, MML, APL, WDX, TZ and ZTL performed the bioinformatics analyses. JYJ, ZHL and ZTL prepared the main figures. JYJ, TZ, ZTL, NS and WJL wrote the manuscript. All authors read and approved the final manuscript.
Corresponding authors
Ethics declarations
Conflict of interest
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
Ethics approval
This article does not contain any studies with human participants or animals performed by any of the authors.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Jiao, JY., Lian, ZH., Liu, ZT. et al. Genome-based reclassification of the genus Meiothermus along with the proposal of a new genus Allomeiothermus gen. nov. Antonie van Leeuwenhoek 115, 645–659 (2022). https://doi.org/10.1007/s10482-022-01723-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10482-022-01723-x