Abstract
A bacterial strain, Gram-stain negative, rod-shaped, aerobic and cellulose-degrading, designated NEAU-DD11T, was isolated from rhizosphere soil of rice collected from Northeast Agricultural University in Harbin, Heilongjiang Province, North-east China. Base on 16S rRNA gene sequence analysis, strain NEAU-DD11T belongs to the genus Massilia and shared high sequence similarities with Massilia phosphatilytica 12-OD1T (98.46%) and Massilia putida 6NM-7 T (98.41%). Phylogenetic analysis based on the 16S rRNA gene and whole genome sequences indicated that strain NEAU-DD11T formed lineage related to M. phosphatilytica 12-OD1T and M. putida 6NM-7 T. The major fatty acids of the strain were C16:0, C17:0-cyclo and C16:1ω7c. The respiratory quinone was Q-8. The polar lipids profile of the strain showed the presence of diphosphatidylglycerol, phosphatidylglycerol, phosphatidylethanolamine, an unidentified polar lipid and an unidentified phospholipid. In addition, the digital DNA-DNA hybridization values between strain NEAU-DD11T and M. phosphatilytica 12-OD1T and M. putida 6NM-7 T were 45.4 and 35.6%, respectively, which are lower than the accepted threshold value of 70%. The DNA G + C content of strain NEAU-DD11T was 66.2%. The whole genome analysis showed the strain contained carbohydrate enzymes such as glycoside hydrolase and polysaccharide lyase, which enabled the strain to have the function of degrading cellulose. On the basis of the phenotypic, genotypic and chemotaxonomic characteristics, we conclude that strain NEAU-DD11T represents a novel species of the genus Massilia, for which the name Massilia cellulosiltytica sp. nov. is proposed. The type strain is NEAU-DD11T (= CCTCC AB 2019141 T = DSM 109721 T).
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Data availability
The GenBank/EMBL/DDBJ accession number for the 16S rRNA gene sequence of strain NEAU-DD11T is MN784464. The Whole Genome Shotgun project has been deposited at DDBJ/ENA/GenBank under the accession WSES00000000. The version described in this paper is version WSES00000000.1.
Abbreviations
- CCTCC:
-
China Center for Type Culture Collection
- DSM:
-
Deutsche Sammlung von Mikroorganismen und Zellkulturen
- GDMCC:
-
Guangdong Microbial Culture Collection Center
- DPG:
-
Diphosphatidylglycerol
- PE:
-
Phosphatidylethanolamine
- PG:
-
Phosphatidylglycerol
- MEGA:
-
Molecular Evolutionary Genetics Analysis
- ANI:
-
Average nucleotide identity
- dDDH:
-
Digital DNA-DNA hybridization
- GGDC:
-
Genome-to-Genome Distance Calculator
- TYGS:
-
Type strain Genome Server
- ISCC-NBS:
-
Inter-society color council-national bureau of standards
- GO:
-
Gene Ontology
- KEGG:
-
Kyoto Encyclopedia of Genes and Genome
- CAZy:
-
Carbohydrate-Active enZYmes Database
References
Cantarel BL, Coutinho PM, Rancurel C, Bernard T, Lombard V, Henrissat B (2009) The Carbohydrate-Active EnZymes database (CAZy): an expert resource for glycogenomics. Nucleic Acids Res 37(suppl 1):D233–D238
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 104:1601–1609
Chaudhary DK, Kim J (2017) Massilia agri sp. nov., isolated from reclaimed grassland soil. Int J Syst Evol Microbiol 67:2696–2703
Chen L, Xiong Z, Sun L, Yang J, Jin Q (2012) VFDB 2012 update: toward the genetic diversity and molecular evolution of bacterial virulence factors. Nucleic Acids Res 40(D1):D641–D645
Chun J, Rainey FA (2014) Integrating genomics into the taxonomy and systematics of the Bacteria and Archaea. Int J Syst Evol Microbiol 64:316–324
Collins MD (1985) Isoprenoid quinone analyses in bacterial classification and identification. In: Goodfellow M, Minnikin DE (eds) Chemical methods in bacterial systematics. Academic Press, London, pp 267–284
Du Y, Yu X, Wang GJ (2012) Massilia tieshanensis sp. Nov., isolated from mining soil. Int J Syst and Evol Microbiol 62(10):2356–2362
Embley TM (1991) The linear PCR reaction: a simple and robust method for sequencing amplified rRNA genes. Lett Appl Microbiol 13:171–174
Felsenstein J (1981) Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol 17:368–376
Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Mol Biol Evol 39:783–791
Gallego V, Sánchez-Porro C, García MT, Ventosa A (2006) Massilia aurea sp. nov., isolated from drinking water. Int J Syst Evol Microbiol 56:2449–2453
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 105:307–315
Guang DF, Song ZY, Hua PL, Hong HZ (2016) Massilia putida sp. nov., a dimethyl disulfide-producing bacterium isolated from wolfram mine tailing. Int J Syst Evol Microbiol 66:50–55
Guo BX, Liu YQ, Gu ZQ, Shen L, Liu KS, Wang NL, Xing TT, Liu HC, Zhou YG, Li JL (2016) Massilia psychrophila sp. nov., isolated from an ice core. Int J Syst Evol Microbiol 66:4088–4093
Kämpfer P, Falsen E, Busse HJ (2008) Naxibacter varians sp. Nov. and Naxibacter haematophilus sp. Nov., and emended description of the genus Naxibacter. Int J Syst Evol Microbiol 58(7):1680–1684
Kämpfer P, Lodders N, Martin K, Falsen E (2012) Massilia oculi sp. nov., isolated from a human clinical specimen. Int J Syst Evol Microbiol 62:364–369
Kelly KL (1964) Inter-society colour council-national bureau of standards colour-name charts illustrated with centroid colours published in US
Kikuchi M, Konno N, Suzuki T, Fujii Y, Kodama Y, Isogai A, Habu N (2020) A bacterial endo-β-1,4-glucuronan lyase, CUL-I from Brevundimonas sp SH203, belonging to a novel polysaccharide lyase family. Protein Expr Purif 166:105502
Kim DU, Ka JO (2014) Roseomonas soli sp. nov., isolated from an agricultural soil cultivated with Chinese cabbage (Brassica campestris). Int J Syst Evol Microbiol 64:1024–1029
Kim J (2014) Massilia kyonggiensis sp. nov., isolated from forest soil in Korea. Int J Syst Evol Microbiol 52:378–383
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
La Scola B, Birtles RJ, Mallet MN, Raoult D (1998) Massilia timonae gen. nov., sp. nov., isolated from blood of an immunocompromised patient with cerebellar lesions. J Clin Microbiol 36:2847–2852
Lányi B (1987) Classical and rapid identification methods for medically important bacteria. Methods Microbiol 19:1–67
Lee H, Kim DU, Park S, Yoon JH, Ka JO (2017) Massilia chloroacetimidivorans sp. Nov., a chloroacetamide herbicide-degrading bacterium isolated from soil. Antonie Van Leeuwenhoek 110(6):751–758
Li R, Li Y, Kristiansen K, Wang J (2008) SOAP: short oligonucleotide alignment program. Bioinformatics 24(5):713–714
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 20:265–272
Liu B, Pop M (2009) ARDB-antibiotic resistance genes database. Nucleic Acids Res 37(suppl1):D443–D447
Lu HB, Deng TC, Xu MY (2020) Massilia aquatica sp. nov., Isolated from a Subtropical Stream in China. Curr Microbiol 77:3185–3191
Medema MH, Blin K, Cimermancic P, de Jager V, Zakrzewski P, Fischbach MA, Weber T, Takano E, Breitling R (2011) antiSMASH: rapid identification, annotation and analysis of secondary metabolite biosynthesis gene clusters in bacterial and fungal genome sequences. Nucleic Acids Res 39(suppl 2):W339–W346
Meier-Kolthoff JP, Auch AF, Klenk HP, Goker M (2013) Genome sequence-based species delimitation with confidence intervals and improved distance functions. BMC Bioinform 14:60
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
Minnikin DE, O’Donnell AG, Goodfellow M, Alderson G, Athalye M, Schaal K, Parlett JH (1984) An integrated procedure for the extraction of bacterial isoprenoid quinones and polar lipids. J Microbiol Methods 2:233–241
Nikodinovic J, Barrow KD, Chuck JA (2003) High yield preparation of genomic DNA from Streptomyces. Biotechniques 35:932–934
Raths R, Peta V, Bücking H (2020) Massilia arenosa sp. Nov., isolated from the soil of a cultivated maize field. Int J Syst Evol Microbiol 70(6):3912–3920
Richter M, Rossello-Mora R (2009) Shifting the genomic gold standard for the prokaryotic species definition. Proc Natl Acad Sci USA 106:19126–19131
Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425
Shen L, Liu YQ, Wang NL, Yao TD, Jiao NZ, Liu HC, Zhou YG, Xu BQ, Liu XB (2013) Massilia yuzhufengensis sp. nov., isolated from an ice core. Int J Syst Evol Microbiol 263:1285–1290
Singh H, Du J, Won K, Yang JE, Yin C, Kook MC, Yi TH (2015) Massilia arvi sp. nov., isolated from fallow-land soil previously cultivated with Brassica oleracea, and emended description of the genus Massilia. Int J Syst Evol Microbiol 65:3690–3696
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, DC, pp 607–654
Stackebrandt E, Ebers J (2006) Taxonomic parameter revisited: tarnished gold standards. Microbiol Today 33:152–155
Sudhir K, Glen S, Michael Li, Christina K, Koichiro T (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35(6):1547–1549
Suleiman M, Krüger A, Antranikian G (2020) Biomass-degrading glycoside hydrolases of archaeal origin. Biotechnol Biofuels 13:153. https://doi.org/10.1186/s13068-020-01792-y
Sun LN, Yang ED, Cui DX, Ni YW, Wang YB, Sun DD, Wang WY (2017) Massilia buxea sp. nov., isolated from a rock surface. Int J Syst Evol Microbiol 67:4390–4396
Teather RM, Wood PJ (1982) Use of congo red-polysaccharide interactions in enumeration and characterization of cellulolytic bacteria from the bovine rumen. Appl Environ Microbiol 43(4):777–780
Wang HS, Zhang XX, Wang SY, Zhao BS, Lou K, Xing XH (2018) Massilia violaceinigra sp. nov., a novel purple-pigmented bacterium isolated from glacier permafrost. Int J Syst Evol Microbiol 68:2271–2278
Wayne LG, Brenner DJ, Colwell RR, Grimont PAD, Kandler O, Krichevsky MI, Moore LH, Moore WEC, Murray RGE (1987) International Committee on Systematic Bacteriology. Report of the ad hoc committee on reconciliation of approaches to bacterial systematics. Int J Syst Bacteriol 37:463–464
Weon HY, Kim BY, Hong SB, Jeon YA, Koo BS, Kwon SW, Stackebrandt E (2009) Massilia niabensis sp. nov. and Massilia niastensis sp. nov., isolated from air samples. Int J Syst Evol Microbiol 59:1656–1660
Weon HY, Kim BY, Son JA, Jang HB, Hong SK, Go SJ, Kwon SW (2008) Massilia aerilata sp. nov., isolated from an air sample. Int J Syst Evol Microbiol 58:1422–1425
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 61:1165–1169
Yang ED, Zhao MY, Li SS, Wang YX, Sun LN, Liu J, Wang WY (2019) Massilia atriviolacea sp. nov., a dark purple-pigmented bacterium isolated from soil. Int J Syst Evol Microbiol 69:2135–2141
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
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 110:1281–1286
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. Microorg 7(9):360
Zhao JW, Yu B, Han CY, Cao P, Yu ZY, Ju HX, Xiang WS, Wang XJ (2020) Microbispora fusca sp. Nov., a novel actinomycete isolated from the ear of wheat (Triticum aestivum L.). Int J Syst Evol Microbiol 70(1):139–145
Zheng BX, Bi QF, Hao XL, Zhou GW, Yang XR (2017) Massilia phosphatilytica sp. nov., a phosphate solubilizing bacteria isolated from a long-term fertilized soil. Int J Syst Evol Microbiol 67:2514–2519
Zu D, Wanner G, Overmann J (2008) Massilia brevitalea sp. nov., a novel betaproteobacterium isolated from lysimeter soil. Int J Syst Evol Microbiol 58:1245–1251
Acknowledgements
The authors would like to thank Prof. Aharon Oren (Department of Plant and Environmental Sciences, the Alexander Silberman Institute of Life Sciences, the Hebrew University of Jerusalem) for helpful advice on the specific epithet.
Funding
This work was supported in part by grants from the Key Program of the National Natural Science Foundation of China (No. 32030090), the China Postdoctoral Science Foundation (2018M631907) and the Heilongjiang Postdoctoral Fund (LBH-Z17015).
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Chuanjiao Du performed the laboratory experiments, analyzed the data, and drafted the manuscript. Chenxu Li contributed to the biochemical characterization. Peng Cao contributed to the morphological analyzes. Tingting Li contributed to the fatty acids determination. Dandan Du contributed to the polyphasic taxonomy. Xiangjing Wang participated to the discussions of each section of experiments. Junwei Zhao and Wensheng Xiang designed the experiments and revised the manuscript.
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Du, C., Li, C., Cao, P. et al. Massilia cellulosiltytica sp. nov., a novel cellulose-degrading bacterium isolated from rhizosphere soil of rice (Oryza sativa L.) and its whole genome analysis. Antonie van Leeuwenhoek 114, 1529–1540 (2021). https://doi.org/10.1007/s10482-021-01618-3
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DOI: https://doi.org/10.1007/s10482-021-01618-3