Abstract
A Gram-positive, motile, rod-shaped and lignin-degrading novel actinomycete, designated strain NEAU-YY56T, was isolated from the rhizosphere soil of wheat (Triticum aestivum L.) collected from Zhumadian, Henan Province, Central China and characterized using a polyphasic approach. Phylogenetic analysis based on the 16S rRNA gene sequence indicated that strain NEAU-YY56T belonged to the genus Cellulomonas and exhibited 16S rRNA gene sequence similarities of 98.7, 98.2 and 98.1% to Cellulomonas pakistanensis JCM 18755T, Cellulomonas denverensis JCM 14733T and Cellulomonas hominis JCM 12133T, respectively. The whole-cell sugars were glucose, rhamnose and ribose. The peptidoglycan of strain NEAU-YY56T contained ornithine and glutamic acid. The phospholipid profile was found to contain diphosphatidylglycerol, phosphatidylethanolamine, phosphatidylinositol mannoside and two unknown glycolipids. The major menaquinone was MK-9(H4). The major fatty acids (> 5.0%) were identified as anteiso-C15:0, C16:0, C14:0 and anteiso-C17:0. Meanwhile, DNA G+C content was 74.7%. The morphological and chemotaxonomic properties of strain NEAU-YY56T were also confirmed the affiliation of the isolate to the genus Cellulomonas. However, physiological and biochemical characteristics indicated that strain NEAU-YY56T can be clearly differentiated from its closest relatives. In addition, the ANI values and dDDH levels between strain NEAU-YY56T and related Cellulomonas species were lower than the accepted threshold value. Therefore, it is concluded that strain NEAU-YY56T represents a novel species of the genus Cellulomonas, for which the name Cellulomonas triticagri sp. nov. is proposed. The type strain is NEAU-YY56T (= DSM 106717T = JCM 32550T).
Similar content being viewed by others
Abbreviations
- Ala:
-
Alanine
- ANI:
-
Average nucleotide identity
- Asp:
-
Aspartic acid
- atpD:
-
ATP synthase F1, beta subunit
- dDDH:
-
Digital DNA:DNA hybridization
- DPA:
-
Dulcitol-proline agar
- DPG:
-
Diphosphatidylglycerol
- DSM:
-
Deutsche Sammlung von Mikroorganismen und Zellkulturen
- GC–MS:
-
Gas Chromatography–Mass Spectrometry
- GL:
-
Unknown glycolipid
- Glu:
-
Glutamic acid
- GO:
-
Gene Ontology
- gyrB:
-
DNA gyrase subunit B
- ISCC-NBS:
-
Inter-Society Color Council-National Bureau of Standards
- ISP:
-
International Streptomyces Project
- ISP 2:
-
Yeast extract–malt extract agar
- ISP 3:
-
Oatmeal agar
- ISP 4:
-
Inorganic salt-starch agar
- ISP 5:
-
Glycerol-asparagine agar
- ISP 6:
-
Peptone-yeast extract iron agar
- ISP 7:
-
Tyrosine agar
- JCM:
-
Japan Collection of Microorganisms
- KEGG:
-
Kyoto Encyclopedia of Genes and Genomes
- MEGA:
-
Molecular Evolutionary Genetics Analysis
- MLSA:
-
Multilocus sequence analysis
- Orn:
-
Ornithine
- PE:
-
Phosphatidylethanolamine
- PGAP:
-
Prokaryotic Genome Annotation Pipeline
- PIM:
-
Phosphatidylinositol mannoside
- recA:
-
Recombinase A
- relA:
-
PpGpp synthetase
- rpoB:
-
RNA polymerase, beta subunit
- TSA:
-
Trypticase soy agar
- TSB:
-
Trypticase soy both
References
Ahmed I, Kudo T, Abbas S, Muhammad E, Takao I, Toru F, Moriya O (2014) Cellulomonas pakistanensis sp. Nov. a moderately halotolerant Actinobacteria. Int J Syst Evol Microbiol 64(Pt_7):2305–2311. https://doi.org/10.1099/ijs.0.059063-0
Bergey DH, Harrison FC, Breed RS, Hammer BW, Huntoon FM (1923) Bergey’s manual of determinative bacteriology. Williams & Wilkins, Baltimore
Blánquez A, Ball AS, González-Pérez JA, Jiménez-Morillo NT, González-Vila F, Arias ME, Hernandez M (2017) Laccase SilA from Streptomyces ipomoeae CECT 3341, a key enzyme for the degradation of lignin from agricultural residues? PLoS ONE 12(11):e0187649. https://doi.org/10.1371/journal.pone.0187649
Cao P, Liu CX, Sun PY, Fu XP, Wang SX, Wu FZ, Wang XJ (2016) An endophytic Streptomyces sp. strain DHV3–2 from diseased root as a potential biocontrol agent against Verticillium dahliae and growth elicitor in tomato (Solanum lycopersicum). Antonie Van Leeuwenhoek 109(12):1573–1582. https://doi.org/10.1007/s10482-016-0758-6
Cao P, Li CX, Tan KF, Liu CZ, Xu X, Zhang SY, Wang XJ, Zhao JW, Xiang WS (2020) Characterization, phylogenetic analyses and pathogenicity of Enterobacter cloacae on rice seedlings in Heilongjiang Province, China. Plant Dis 104(6):1601–1609. https://doi.org/10.1094/PDIS-12-19-2557-RE
Chun J, Rainey FA (2014) Integrating genomics into the taxonomy and systematics of the Bacteria and Archaea. Int J Syst Evol Microbiol 64(Pt_2):316–324. https://doi.org/10.1099/ijs.0.054171-0
Collins MD (1985) Chemical methods in bacterial systematics. In: Goodfellow M, Minnikin DE (eds) Isoprenoid quinone analyses in bacterial classification and identification. Academic Press, London, pp 267–284
Felsenstein J (1981) Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol 17(6):368–376. https://doi.org/10.1007/BF01734359
Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39(4):783–791. https://doi.org/10.1111/j.1558-5646.1985.tb00420.x
Gao RX, Liu CX, Zhao JW, Jia FY, Yu C, Yang LY, Wang XJ, Xiang WS (2014) Micromonospora jinlongensis sp. nov., isolated from muddy soil in China and emended description of the genus Micromonospora. Antonie Van Leeuwenhoek 105(2):307–315. https://doi.org/10.1007/s10482-013-0074-3
Gordon RE, Barnett DA, Handerhan JE, Pang C (1974) Nocardia coeliaca, Nocardia autotrophica, and the nocardin strain. Int J Syst Bacteriol 24(1):54–63. https://doi.org/10.1099/00207713-24-1-54
Hasegawa T, Takizawa M, Tanida S (1983) A rapid analysis for chemical grouping of aerobic actinomycetes. J Gen Appl Microbiol 29(4):319–322. https://doi.org/10.2323/jgam.29.319
Kelly KL (1964) Inter-society color council-national bureau of standards color-name charts illustrated with centroid colors published in US
Kim SB, Brown R, Oldfield C, Gilbert SC, Iliarionov S, Goodfellow M (2000) Gordonia amicalis sp. nov., a novel dibenzothiophene-desulphurizing actinomycete. Int J Syst Evol Microbiol 50(6):2031–2036. https://doi.org/10.1099/00207713-50-6-2031
Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16(2):111–120. https://doi.org/10.1007/BF01731581
Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35(6):1547–1549. https://doi.org/10.1093/molbev/msy096
Lechevalier MP, Lechevalier HA (1980) The chemotaxonomy of actinomycetes. In: Dietz A, Thayer DW (eds) Actinomycete taxonomy special publication, vol 6. Society of Industrial Microbiology, Arlington, pp 227–291
Li R, Li Y, Kristiansen K, Wang J (2008) SOAP: short oligonucleotide alignment program. Bioinformatics 24(5):713–714. https://doi.org/10.1093/bioinformatics/btn025
Li R, Zhu H, Ruan J, Qian W, Fang X, Shi Z, Li Y, Li S, Shan G, Kristiansen K, Li S, Yang H, Wang J, Wang J (2010) De novo assembly of human genomes with massively parallel short read sequencing. Genome Res 20(2):265–272. https://doi.org/10.1101/gr.097261.109
Li YQ, Zhang H, Xiao M, Dong ZY, Zhang JY, Narsing Rao MP, Li WJ (2020) Cellulomonas endophytica sp. nov., isolated from Gastrodia elata Blume. Int J Syst Evol Microbiol 70(5):3091–3095. https://doi.org/10.1099/ijsem.0.004133
Meier-Kolthoff JP, Göker M (2019) TYGS is an automated high-throughput platform for state-of-the-art genome-based taxonomy. Nat Commun 10(1):2182. https://doi.org/10.1038/s41467-019-10210-3
Meier-Kolthoff JP, Sardà Carbasse J, Peinado-Olarte RL, Göker M (2022) TYGS and LPSN: a database tandem for fast and reliable genome-based classification and nomenclature of prokaryotes. Nucleic Acid Res 50(D1):D801–D807. https://doi.org/10.1093/nar/gkab902
Minnikin DE, O’Donnell AG, Goodfellow M, Alderson G, Athalye M, Schaal A, Parlett JH (1984) An integrated procedure for the extraction of bacterial isoprenoid quinones and polar lipids. J Microbiol Methods 2(5):233–241. https://doi.org/10.1016/0167-7012(84)90018-6
Nikodinovic J, Barrow KD, Chuck JA (2003) High yield preparation of genomic DNA from Streptomyces. Biotechniques 35(5):932–934. https://doi.org/10.2144/03355bm05
Richter M, Rossello-Mora R (2009) Shifting the genomic gold standard for the prokaryotic species definition. Proc Natl Acad Sci USA 106(45):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(4):406–425. https://doi.org/10.1093/oxfordjournals.molbev.a040454
Salam N, Jiao J, Zhang X, Li WJ (2020) Update on the classification of higher ranks in the phylum Actinobacteria. Int J Syst Evol Microbiol 70(2):1331–1355. https://doi.org/10.1099/ijsem.0.003920
Shirling EB, Gottlieb D (1966) Methods for characterization of Streptomyces species. Int J Syst Bacteriol 16(3):313–340. https://doi.org/10.1099/00207713-16-3-313
Smibert RM, Krieg NR (1994) Phenotypic characterisation. In: Gerhardt P, Murray RGE, Wood WA, Krieg NR (eds) Methods for general and molecular bacteriology. American Society for Microbiology, pp 607–654. https://doi.org/10.1002/food.19960400226
Stackebrandt E, Schumann P (1986) Genus I. Cellulomonas, Bergey, Harrison, Breed, Hammer and Huntoon 1923, 154 emend. mut. char. Clark 1952, 50 AL. In: Goodfellow M, Kämpfer P, Busse HJ, Trujillo ME, Suzuki K et al (eds) Bergey’s manual of systematic bacteriology, vol 5, 2nd edn. Springer, NewYork, pp 702–710
Stackebrandt E, Schumann P, Prauser H (2006) The prokaryotes: a handbook on the biology of bacteria. The family Cellulomonadaceae, New York, pp 983–1001. https://doi.org/10.1007/0-387-30743-5_40
Wayne LG, BrennerDJ CRR, Grimont PAD, Kandler O, Krichevsky MI, Moore LH, Moore WEC, Murray RGE, Stackebrandt E, Starr MP, Trüper HG (1987) Report of the ad hoc committee on reconciliation of approaches to bacterial systematics. Int J Syst Bacteriol 37(4):463–464. https://doi.org/10.1099/00207713-37-4-463
Wu C, Lu X, Qin M, Wang Y, Ruan J (1989) Analysis of menaquinone compound in microbial cells by HPLC. Microbiology 16:176–178
Xiang WS, Liu CX, Wang XJ, Du J, Xi LJ, Huang Y (2011) Actinoalloteichus nanshanensis sp. nov., isolated from the rhizosphere of a fig tree (Ficus religiosa). Int J Syst Evol Microbiol 61(5):1165–1169. https://doi.org/10.1099/ijs.0.023283-0
Xu CY, Singh D, Dorgan KM, Zhang XY, Chen SL (2015) Screening of ligninolytic fungi for biological pretreatment of lignocellulosic biomass. Can J Microbiol 61(10):745–752. https://doi.org/10.1139/cjm-2015-0156
Yokota A, Tamura T, Hasegawa T, Huang LH (1993) Catenuloplanes japonicas gen. nov., sp. nov., nom. rev., a new genus of the order Actinomycetales. Int J Syst Bacteriol 43(4):805–812. https://doi.org/10.1099/00207713-43-4-805
Yoon SH, Ha SM, Kwon S, Lim J, Kim Y, Seo H, Chun J (2017a) Introducing EzBioCloud: a taxonomically united database of 16S rRNA and whole genome assemblies. Int J Syst Evol Microbiol 67(5):1613–1617. https://doi.org/10.1099/ijsem.0.001755
Yoon SH, Ha SM, Lim J, Kwon S, Chun J (2017b) A large-scale evaluation of algorithms to calculate average nucleotide identity. Antonie Van Leeuwenhoek 110(10):1281–1286. https://doi.org/10.1007/s10482-017-0844-4
Zhang H (2006) New Advance of study on ligninolytic enzymes. Tianjin Agric Sci 3:8–12
Zhao JW, Shi LL, Li WC, Wang JB, Wang H, Tian YY, Xiang WS, Wang XJ (2018) Streptomyces tritici sp. nov. a novel actinomycete isolated from rhizosphere soil of wheat (Triticum aestivum L.). Int J Syst Evol Microbiol 68(2):492–497. https://doi.org/10.1099/ijsem.0.002493
Zhao JW, Han LY, Yu MY, Cao P, Li DM, Guo XW, Liu YQ, Wang XJ, Xiang WS (2019) Characterization of Streptomyces sporangiiformans sp. nov., a Novel Soil Actinomycete with Antibacterial Activity against Ralstonia solanacearum. Microorganisms 7(9):360. https://doi.org/10.3390/microorganisms7090360
Acknowledgements
This work was supported in part by grants from the Youth Scientific Research Fund of Liaoning University (LDQN-202010), People's Livelihood Science and Technology Program of Liaoning Provincial Department of Science and Technology (2021JH2/10200015), and General Research Project Found of Liaoning Province Education Department (LJC201910). We are grateful to Professor Aharon Oren (The Hebrew University of Jerusalem) for helpful advice on the epithet.
Funding
This work was funded by Youth Scientific Research Fund of Liaoning University (Grant No. LDQN-202010), People's Livelihood Science and Technology Program of Liaoning Provincial Department of Science and Technology (Grant No. 2021JH2/10200015), General Research Project Found of Liaoning Province Education Department (Grant no. LJC201910).
Author information
Authors and Affiliations
Contributions
CH and YZ performed the laboratory experiments, analyzed the data, and drafted the manuscript. BY contributed to the biochemical characterization. QS and YT contributed to the morphological analyzes. HS contributed to the fatty acids determination. YZ contributed to the Genomic analysis. JZ participated to the discussions of each section of experiments. WX and CZ designed the experiments and revised the manuscript.
Corresponding authors
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Ethical standards
This article does not contain any studies with human participants and/or animals performed by any of the authors. The formal consent is not required in this study.
Additional information
Communicated by Erko Stackebrandt.
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
Han, C., Zhang, Y., Yu, B. et al. Cellulomonas triticagri sp. nov., isolated from the rhizosphere soil of wheat (Triticum aestivum L.). Arch Microbiol 204, 449 (2022). https://doi.org/10.1007/s00203-022-03036-z
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00203-022-03036-z