Abstract
A Gram-staining-negative, aerobic, and rod-shaped with tapered end myxobacterium, designed as strain H56D21T, was isolated from forest soil sampled from the Diaoluo Mountain National Nature Reserve located in Hainan Province, PR China. It showed prey ability on two kinds of phytopathogens including both fungi (Fusarium solani, Fusarium graminearum, and Fusarium oxysporum) and bacteria (Ralstonia solanacearum and Xanthomonas campestris). Phylogenetic analyses based on the 16S rRNA gene and core genes sequences revealed that strain H56D21T belonged to the genus Hyalangium and was most closely related to Cystobacter gracilis DSM 14753 T and Hyalangium minutum DSM 14724 T. Genome comparison showed 85.6% and 82.3% of average nucleotide identity between strain H56D21T and the above two type strains and 29.8% and 25.1% of digital DNA-DNA hybridization , respectively. The novel strain had a large genome size of 13.56 Mbp and a high DNA G + C content of 67.1%. Genome annotation identified 46 secondary metabolite biosynthesis gene clusters and 187 CAZymes-encoding genes. The major fatty acids contained iso-C15:0, iso-C15:0 DMA, C16:1 ω5c, and iso-C17:0. The dominant respiratory quinone was menaquinone 8. Based on the phenotypic, chemotaxonomic and phylogenetic analyses, we suggested that strain H56D21T should represent a novel species of the genus Hyalangium with a proposed name of Hyalangium versicolor sp. nov. (type strain H56D21T = GDMCC 1.1944 T = KCTC 82613 T) and Cystobacter gracilis should be reclassified as Hyalangium gracile 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
The GenBank/EMBL/DDBJ accession number for the 16S rRNA gene of strain H56D21T is MZ577175. The whole genome shotgun projects for strain H56D21T, Cystobacter gracilis DSM 14753 T and Stigmatella hybrida DSM 14722 T have been deposited in GenBank database under the accession numbers of JAHXBF000000000, JAHXBG000000000 and JAHXBH000000000, respectively.
Abbreviations
- ANI:
-
Average nucleotide identity
- dDDH:
-
Digital DNA-DNA hybridization
- NJ:
-
Neighbor-joining
- MP:
-
Maximum-parsimony
- ML:
-
Maximum likelihood
- UBCG:
-
Up-to-data bacteria core
- BGCs:
-
Biosynthetic gene clusters
- DMA:
-
Dimethylacetal
References
Aziz RK, Bartels D, Best AA, DeJongh M, Disz T et al (2008) The RAST server: rapid annotations using subsystems technology. BMC Genomics 9:75. https://doi.org/10.1186/1471-2164-9-75
Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M et al (2012) SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 19:455–477. https://doi.org/10.1089/cmb.2012.0021
Chambers J, Sparks N, Sydney N, Livingstone PG, Cookson AR et al (2020) Comparative genomics and pan-genomics of the Myxococcaceae, including a description of five novel species: Myxococcus eversor sp. nov., Myxococcus llanfairpwllgwyngyllgogerychwyrndrobwllllantysiliogogogochensis sp. nov., Myxococcus vastator sp. nov., Pyxidicoccus caerfyrddinensis sp. nov., and Pyxidicoccus trucidator sp. nov. Genome Biol Evol 12:2289–2302. https://doi.org/10.1093/gbe/evab040
Collins MD, Pirouz T, Goodfellow M, Minnikin DE (1977) Distribution of menaquinones in actinomycetes and corynebacteria. J Gen Microbiol 100:221–230. https://doi.org/10.1099/00221287-100-2-221
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
Garcia RO, Reichenbach H, Ring MW, Müller R (2009) Phaselicystis flava gen. nov. sp. nov. an arachidonic acid-containing soil myxobacterium, and the description of Phaselicystidaceae fam. nov. Int J Syst Evol Microbiol 59:1524–1530. https://doi.org/10.1099/ijs.0.003814-0
Garcia R, Gerth K, Stadler M, Dogma IJ Jr, Muller R (2010) Expanded phylogeny of myxobacteria and evidence for cultivation of the ‘unculturables.’ Mol Phylogenet Evol 57:878–887. https://doi.org/10.1016/j.ympev.2010.08.028
Garcia R, Gemperlein K, Müller R (2014) Minicystis rosea gen. nov. sp. nov. a polyunsaturated fatty acid-rich and steroid-producing soil myxobacterium. Int J Syst Evol Microbiol 64:3733–3742. https://doi.org/10.1099/ijs.0.068270-0
Gemperlein K, Rachid S, Garcia RO, Wenzel SC, Müller R (2014) Polyunsaturated fatty acid biosynthesis in myxobacteria: different PUFA synthases and their product diversity. Chem Sci 5:1733–1741. https://doi.org/10.1039/c3sc53163e
Goris J, Konstantinidis KT, Klappenbach JA, Coenye T, Vandamme P et al (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
Kai B, Simon S, Alexander MK, Zach CP, Gilles PW et al (2021) antiSMASH 6.0: improving cluster detection and comparison capabilities. Nucleic Acids Res 49:29–35. https://doi.org/10.1093/nar/gkab335
Kazumori M, Wataru I (2020) Environmental atlas of prokaryotes enables powerful and intuitive habitat-based analysis of community structures. iScience 23:101624. https://doi.org/10.1016/j.isci.2020.101624
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
Livingstone PG, Ingleby O, Girdwood S, Cookson AR, Morphew RM et al (2020) Predatory organisms with untapped biosynthetic potential: descriptions of novel Corallococcus species C. aberystwythensis sp. nov., C. carmarthensis sp. nov., C. exercitus sp. nov., C. interemptor sp. nov., C. llansteffanensis sp. nov., C. praedator sp. nov., C. sicarius sp. nov., and C. terminator sp. nov. Appl Environ Microbiol 86:e01931-e2019. https://doi.org/10.1128/AEM.01931-19
McCurdy HD (1969) Studies on the taxonomy of the Myxobacterales. I. Record of Canadian isolates and survey of methods. Can J Microbiol 15:1453–1461. https://doi.org/10.1139/m69-259
Meier-Kolthoff JP, Auch AF, Klenk HP, Göker M (2013) Genome sequence-based species delimitation with confidence intervals and improved distance functions. BMC Bioinformatics 14:60. https://doi.org/10.1186/1471-2105-14-60
Na SI, Kim YO, Yoon SH, Ha SM, Baek I, Chun J (2018) UBCG: up-to-date bacterial core gene set and pipeline for phylogenomic tree reconstruction. J Microbiol 56:280–285. https://doi.org/10.1007/s12275-018-8014-6
Nadmid S, Plaza A, Lauro G, Garcia R, Bifulco G et al (2014) Hyalachelins A-C, unusual siderophores isolated from the terrestrial myxobacterium Hyalangium minutum. Org Lett 16:4130–4133. https://doi.org/10.1021/ol501826a
Okanya PW, Mohr KI, Gerth K, Steinmetz H, Huch V et al (2012) Hyaladione, an S-methyl cyclohexadiene-dione from Hyalangium minutum. J Nat Prod 75:768–770. https://doi.org/10.1021/np200776v
Okanya PW, Mohr KI, Gerth K, Kessler W, Jansen R et al (2014) Hyafurones, hyapyrrolines, and hyapyrones: polyketides from Hyalangium minutum. J Nat Prod 77:1420–1429. https://doi.org/10.1021/np500145f
Reichenbach H (2005a) Genus III. Hyalangium gen.nov. In: Brenner DJ, Krieg NR, Staley JT, Garrity GM (eds) Bergey’s Manual of systematic bacteriology (The Proteobacteria), part C (The Alpha-, Beta-, Delta-, and Epsilonproteobacteria). Springer, New York, pp 1099–1101
Reichenbach H (2005b) Genus I. Cystobacter Schroeter 1886, 170AL. In: Brenner DJ, Krieg NR, Staley JT, Garrity GM (eds), Bergey's Manual of Systematic Bacteriology, 2nd edn., vol. 2 (The Proteobacteria), part C (The Alpha-, Beta-, Delta-, and Epsilonproteobacteria), Springer, New York, pp 1086–1096
Richter M, Rossellò-mòra R (2009) Shifting the genomic gold standard for the prokaryotic species definition. Proc Natl Acad Sci USA 106:19126–19131. https://doi.org/10.1073/pnas.0906412106
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
Seemann T (2014) Prokka: rapid prokaryotic genome annotation. Bioinformatics 30:2068–2069. https://doi.org/10.1093/bioinformatics/btu153
Surup F, Chauhan D, Niggemann J, Bartok E, Herrmann J et al (2018) Activation of the NLRP3 inflammasome by Hyaboron, a new asymmetric boron-containing macrodiolide from the myxobacterium Hyalangium minutum. ACS Chem Biol 13:2981–2988. https://doi.org/10.1021/acschembio.8b00659
Waite DW, Chuvochina M, Pelikan C, Parks DH, Yilmaz P et al (2020) Proposal to reclassify the proteobacterial classes Deltaproteobacteria and Oligoflexia, and the phylum Thermodesulfobacteria into four phyla reflecting major functional capabilities. Int J Syst Evol Microbiol 70:5972–6016. https://doi.org/10.1099/ijsem.0.004213
Wang JJ, Ran Q, Du XR, Wu SG, Wang JN et al (2021) Two new Polyangium species, P. aurulentum sp. nov and P. jinanense sp. nov, isolated from a soil sample. Syst Appl Microbiol 44:126274. https://doi.org/10.1016/j.syapm.2021.126274
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
Yoon SH, Ha SM, Kwon S, Lim J, Kim Y et al (2017a) 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
Yoon SH, Ha SM, Lim JM, Kwon SJ, Chun J (2017b) 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 H, Yohe T, Huang L, Entwistle S, Wu P et al (2018) dbCAN2: a meta server for automated carbohydrate-active enzyme annotation. Nucleic Acids Res 46:95–101. https://doi.org/10.1093/nar/gky418
Zhou Y, Yi S, Zang Y, Yao Q, Zhu H (2021) The predatory myxobacterium Citreicoccus inhibens gen. nov. sp. nov Showed antifungal activity and bacteriolytic property against phytopathogens. Microorganisms. 9:2137. https://doi.org/10.3390/microorganisms9102137
Funding
This work was jointly supported by the Natural Science Foundation of China (32000007), the Guangdong Special Support Program (2021JC06N628), the GDAS’ Special Project of Science and Technology Development (2020GDASYL-20200301003) and the Science and Technology Program of Guangdong Province (2021B1212050022).
Author information
Authors and Affiliations
Contributions
XJZ, JLL and XQD: carried out the experiments. XJZ and YL: preformed genome analysis. XJZ, XQD and HHZ: funding acquisition. XJZ: wrote the manuscript. GDF, YL, QY and HHZ: revised the manuscript. All authors read and approved the final manuscript.
Corresponding authors
Ethics declarations
Conflicts of interest
The authors declare that there are no conflicts of interest.
Additional information
Communicated by Wen-Jun Li.
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
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
Zhang, X., Feng, G., Liu, Y. et al. Characterization of phytopathogen-preying Hyalangium versicolor sp. nov., and proposal for the reclassification of Cystobacter gracilis as Hyalangium gracile comb. Nov. Arch Microbiol 205, 198 (2023). https://doi.org/10.1007/s00203-023-03512-0
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00203-023-03512-0