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Puerhibacterium puerhi gen. nov., sp. nov., a novel member of the family Promicromonosporaceae, isolated from Pu-erh tea pile-fermentation

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Abstract

A Gram-staining positive aerobic bacterium, designated TLY-12T, was isolated from the Pu-erh tea pile-fermentation process in Pu'er city, Yunnan, China. Strain TLY-12T grew at 15–37 °C (optimum, 30 °C), pH 6.0–11.0 (optimum, pH 9.0) and 0–9.0% (w/v) NaCl (optimum, 3.0%). The major cellular fatty acids were anteiso-C15:0, C16:0 and iso-C16:0. The respiratory quinone were menaquinones MK-9 (H2) and MK-9 (H4). The polar lipids were phosphatidylglycerol (PG), diphosphatidylglycerol (DPG), phosphatidylinositol (PI), phosphoglycolipid (PGL), glycolipid (GL) and an unidentified phospholipid (PL). The peptidoglycan contained glutamic acid, aspartic acid, alanine and lysine, with the last named being the diagnostic diamino acid. Whole-cell sugars of the isolate were ribose, galactose and glucose. Phylogenetic analyses of 16S rRNA gene showed that this strain belonged to the family Promicromonosporaceae, and was most closely related to Isoptericola cucumis DSM 101603 T, which gave sequence similarity of 97.9%. Genome sequencing revealed a genome size of 3.91 Mbp and a G + C content of 75.0%. Average nucleotide identity and digital DNA–DNA hybridization values were all below the species threshold of described Promicromonosporaceae species. Genome phylogenetic analysis showed that strain TLY-12T formed a separate evolutionary branch, and was parallel to other related genera of Promicromonosporaceae. Based on the phylogenetic, phenotypic, chemotaxonomic and genome pairwise data, strain TLY-12T is considered to represent a novel species in a new genus in the family Promicromonosporaceae, for which the name Puerhibacterium puerhi gen. nov, sp. nov. is proposed. The type strain is TLY-12T (= CGMCC 1.17157T = KCTC 49467T).

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Abbreviations

ANI:

Average nucleotide identity

dDDH:

Digital DNA–DNA hybridization

COG:

Cluster of orthologous groups of proteins

CRISPR:

Clustered regularly interspaced short palindromic repeats

RNA:

Ribonucleic acid

tRNA:

Transfer ribonucleic acid

sRNA:

Small ribonucleic acid

LTR:

Long terminal repeat

LINE:

Long interspersed nuclear elements

SINE:

Short interspersed nuclear elements

RC:

Rolling circle

TR:

Terminal repeat

References

  • Bakalidou A, Kämpfer P, Berchtold M, Kuhnigk T, Wenzel M, König H (2002) Cellulosimicrobium variabile sp. nov., a cellulolytic bacterium from the hindgut of the termite Mastotermes darwiniensis. Int J Syst Evol Microbiol 52:1185–1192

    CAS  PubMed  Google Scholar 

  • Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M, Kulikov AS, Lesin VM, Nikolenko SI, Pham S, Prjibelski AD, Pyshkin AV, Sirotkin AV, Vyahhi N, Tesler G, Alekseyev MA, Pevzner PA (2012) SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 19:455–477

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bernardet JF, Nakagawa Y, Holmes B, Subcommittee on the taxonomy of Flavobacterium and Cytophaga-like bacteria of the International Committee on Systematics of Prokaryotes (2002) Proposed minimal standards for describing new taxa of the family Flavobacteriaceae and emended description of the family. Int J Syst Evol Microbiol 52:1049–1070

    PubMed  Google Scholar 

  • Castresana J (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 17:540–552

    Article  CAS  PubMed  Google Scholar 

  • Cui X, Schumann P, Stackebrandt E, Kroppenstedt RM, Pukall R, Xu L, Rohde M, Jiang C (2004) Myceligenerans xiligouense gen. nov., sp. nov., a novel hyphae-forming member of the family Promicromonosporaceae. Int J Syst Evol Microbiol 54:1287–1293

    Article  CAS  PubMed  Google Scholar 

  • Da Costa MS, Albuquerque L, Nobre MF, Wait R (2011a) The extraction and identification of respiratory lipoquinones of prokaryotes and their use in taxonomy. Methods Microbiol 38:197–206

    Article  Google Scholar 

  • Da Costa MS, Albuquerque L, Nobre MF, Wait R (2011b) The identification of polar lipids in prokaryotes. Method Microbiol 38:165–181

    Article  Google Scholar 

  • Emms DM, Kelly S (2015) OrthoFinder: solving fundamental biases in whole genome comparisons dramatically improves orthogroup inference accuracy. Genome Biol 16:157

    Article  PubMed  PubMed Central  Google Scholar 

  • Evtushenko LI, Levanova GF, Agre NS (1984) Nucleotide composition of DNA and amino acid composition of A4 peptidoglycan in Promicromonospora citrea. Mikrobiologiya 53:519–520

    CAS  Google Scholar 

  • Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791

    Article  PubMed  Google Scholar 

  • Fitch WM (1971) Toward defining the course of evolution: minimum change for a specific tree topology. Syst Zool 20:406–416

    Article  Google Scholar 

  • Galperin MY, Makarova KS, Wolf YI, Koonin EV (2015) Expanded microbial genome coverage and improved protein family annotation in the COG database. Nucleic Acids Res 43:261–269

    Article  Google Scholar 

  • Hamada M, Otoguro M, Yamamura H, Tamura T, Suzuki K, Hayakawa M (2010) Luteimicrobium subarcticum gen. nov., sp. nov., a new member of the suborder Micrococcineae. Int J Syst Evol Microbiol 60:796–800

    Article  PubMed  Google Scholar 

  • Hamada M, Tamura T, Shibata C, Yamamura H, Hayakawa M, Suzuki K (2012) Sediminihabitans luteus gen. nov., sp. nov., a new member of the family Cellulomonadaceae isolated from sea sediment. Anton Leeuw Int J G 102:325–333

    Article  CAS  Google Scholar 

  • Hamada M, Shibata C, Nurkanto A, Ratnakomala S, Lisdiyanti P, Tamura T, Suzuki K (2015) Tropicihabitans flavus gen. nov., sp. nov., a new member of the family Cellulomonadaceae. Anton Leeuw Int J G 107:1299–1306

    Article  CAS  Google Scholar 

  • Heo J, Cho H, Hamada M, Kim JM, Hong SB, Kim SJ, Kwon SW (2020) Xylanimonas allomyrinae sp. nov. isolated from the gut of larva of Allomyrina dichotoma, reclassification of Xylanibacterium ulmi as Xylanimonas ulmi comb. nov. and Xylanimicrobium pachnodae as Xylanimonas pachnodae comb. nov., and emendation of the genus Xylanimonas. Int J Syst Evol Microbiol 70:1924–1930

    Article  CAS  PubMed  Google Scholar 

  • Kämpfer P, Glaeser Stefanie P, Kloepper Joseph W, Hu CH, McInroy John A, Martin K, Busse HJ (2016) Isoptericola cucumis sp. nov., isolated from the root tissue of cucumber (Cucumis sativus). Int J Syst Evol Microbiol 66:2784–2788

    Article  PubMed  Google Scholar 

  • Khan ST, Harayama S, Tamura T, Ando K, Takagi M, Kazuo SY (2009) Paraoerskovia marina gen. nov., sp. nov., an actinobacterium isolated from marine sediment. Int J Syst Evol Microbiol 59:2094–2098

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Kishino H, Hasegawa M (1989) Evaluation of the maximum likelihood estimate of the evolutionary tree topologies from DNA sequence data, and the branching order in hominoidea. J Mol Evol 29:170–179

    Article  CAS  PubMed  Google Scholar 

  • Krasilʼnikov NA, Kalakoutskii LV, Kirillova NF (1961) A new genus of Actinomycetales, Promicromonospora gen. nov. Bull Acad Sci USSR Ser Biol 1:107–112

    Google Scholar 

  • Lane DJ (1991) 16S/23S rRNA sequencing. In: Stackebrandt E, Goodfellow M (eds) Nucleic acid techniques in bacterial systematics. Wiley, Chichester, pp 115–175

    Google Scholar 

  • Lee LK, Foo KY (2013) Recent advances on the beneficial use and health implications of Pu-Erh tea. Food Res Int 53:619–628

    Article  CAS  Google Scholar 

  • Li R, Li Y, Kristiansen K, Wang J (2008) SOAP: short oligonucleotide alignment program. Bioinformatics 24:713–714

    Article  CAS  PubMed  Google Scholar 

  • 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 2:265–272

    Article  Google Scholar 

  • Lin SH, Liao YC (2013) CISA: contig integrator for sequence assembly of bacterial genomes. PLoS ONE 8:e60843

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ludwig W, Strunk O, Westram R, Richter L, Meier H, Yadhukumar BA, Lai T, Steppi S, Jobb G, Förster W, Brettske I, Gerber S, Ginhart AW, Gross O, Grumann S, Hermann S, Jost R, König A, Liss T, Lüssmann R, May M, Nonhoff B, Reichel B, Strehlow R, Stamatakis A, Stuckmann N, Vilbig A, Lenke M, Ludwig T, Bode A, Schleifer KH (2004) Arb: a software environment for sequence data. Nucleic Acids Res 32:1363–1371

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • Minnikin DE, O’Donnell AG, Goodfellow M, Alderson G, Athalye M (1984) An integrated procedure for the extraction of bacterial isoprenoid quinones and polar lipids. J Microbiol Methods 2:233–241

    Article  CAS  Google Scholar 

  • Mohammadipanah F, Hamedi J, Spröer C, Montero-Calasanz M, Schumann P et al (2014) Promicromonospora iranensis sp. nov., an actinobacterium isolated from rhizospheric soil. Int J Syst Evol Microbiol 64:3314–3319

    Article  CAS  PubMed  Google Scholar 

  • Murray R, Doetsch RN, Robinow CF (1994) Determinative and cytological light microscopy. In: Gerhardt P, Murray RGE, Wood WA, Krieg NR (eds) Methods for general and molecular bacteriology. American Society for Microbiology, Washington, DC, pp 21–41

    Google Scholar 

  • Nguyen LT, Schmidt HA, Von Haeseler A, Minh BQ (2015) IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol Biol Evol 32:268–274

    Article  CAS  PubMed  Google Scholar 

  • Nishijima M, Tazato N, Handa Y, Umekawa N, Kigawa R, Sano C, Sugiyama J (2017) Krasilnikoviella muralis gen. nov., sp. nov., a member of the family Promicromonosporaceae, isolated from the Takamatsuzuka Tumulus stone chamber interior and reclassification of Promicromonospora flava as Krasilnikoviella flava comb. nov. Int J Syst Evol Microbiol 67:294–300

    Article  CAS  PubMed  Google Scholar 

  • Piao AL, Feng XM, Nogi Y, Han L, Li Y, Lv J (2016) Sphingomonas qilianensis sp. nov., isolated from surface soil in the permafrost region of Qilian Mountains. China Curr Microbiol 72:363–369

    Article  CAS  PubMed  Google Scholar 

  • Prauser H, Lechevalier MP, Lechevalier H (1970) Description of Oerskovia gen. n. to harbor Orskov’s motile nocardia. Appl Microbiol 19:534

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Richter M, Rosselló-Móra R (2009) Shifting the genomic gold standard for the prokaryotic species definition. Proc Natl Acad Sci USA 106:19126–19131

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rivas R, Sánchez M, Trujillo ME, Zurdo-Piñeiro JL, Mateos PF, Martínez-Molina E, Velázquez E (2003) Xylanimonas cellulosilytica gen. nov., sp. nov., a xylanolytic bacterium isolated from a decayed tree (Ulmus nigra). Int J Syst Evol Microbiol 53:99–103

    Article  CAS  PubMed  Google Scholar 

  • Rivas R, Trujillo ME, Schumann P, Kroppenstedt RM, Sánchez M, Mateos PF, Martínez-Molina E, Velázquez E (2004) Xylanibacterium ulmi gen. nov., sp. nov., a novel xylanolytic member of the family Promicromonosporaceae. Int J Syst Evol Microbiol 54:557–561

    Article  CAS  PubMed  Google Scholar 

  • Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425

    CAS  PubMed  Google Scholar 

  • Salam N, Jiao JY, Zhang XT, Li WJ (2020) Corrigendum: Update on the classification of higher ranks in the phylum Actinobacteria. Int J Syst Evol Microbiol 70:2958

    Article  PubMed  Google Scholar 

  • Sarmiento-Vizcaíno A, González V, Braña Alfredo F, Molina A, Acuña José L, García LA, Blanco G (2015) Myceligenerans cantabricum sp. nov., a barotolerant actinobacterium isolated from a deep cold-water coral. Int J Syst Evol Microbiol 65:1328–1334

    Article  PubMed  Google Scholar 

  • Sasser M (1990) Identification of bacteria by gas chromatography of cellular fatty acids, MIDI Technical Note 101. MIDI Inc, Netwark, DE

    Google Scholar 

  • Schleifer KH, Kandler O (1972) Peptidoglycan types of bacterial cell walls and their taxonomic implications. Bacteriol Rev 36:407–477

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schumann P, Stackebrandt E (2012) The family Promicromonosporaceae. In: Goodfellow M, Kampfer P, Busse HJ, Trujillo ME, Suzuki K et al (eds) Bergey’s manual of systematic bacteriology, vol 5. Springer, New York, pp 995–1019

    Google Scholar 

  • Schumann P, Weiss N, Stackebrandt E (2001) Reclassification of Cellulomonas cellulans (Stackebrandt and Keddie 1986) as Cellulosimicrobium cellulans gen. nov., comb. nov. Int J Syst Evol Microbiol 51:1007–1010

    Article  CAS  PubMed  Google Scholar 

  • Seemann T (2014) Prokka: rapid prokaryotic genome annotation. Bioinformatics 30:2068–2069

    Article  CAS  PubMed  Google Scholar 

  • Sievers F, Wilm A, Dineen D, Gibson Toby J, Karplus K, Li W, Lopez R, McWilliam H, Remmert M, Söding J, Thompson JD, Higgins DG (2011) Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol Syst Biol 7:539

    Article  PubMed  PubMed Central  Google Scholar 

  • Simpson JT, Wong K, Jackman SD, Schein JE, Jones Steven JM, Birol I (2009) ABySS: a parallel assembler for short read sequence data. Genome Res 19:1117

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Google Scholar 

  • Stackebrandt E, Rainey FA, Ward-Rainey NL (1997) Proposal for a new hierarchic classification system, Actinobacteria classis nov. Int J Syst Bacteriol 47:479–491

    Article  Google Scholar 

  • Stackebrandt E, Schumann P, Cui XL et al (2004a) Reclassification of Cellulosimicrobiumvariabile Bakalidoy et al. 2002 as Isoptericola variabilis gen. nov., comb. nov. Int J Syst Evol Microbiol 54:685–688

    Article  CAS  PubMed  Google Scholar 

  • Stackebrandt E, Schumann P et al (2004b) Reclassification of Promicromonospora pachnodea Cazemier as Xylanimicrobium pachnodae gen. nov., comb. nov. Int J Syst Evol Microbiol 54:1383–1386

    Article  CAS  PubMed  Google Scholar 

  • Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol biol Evol 30:2725–3272

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tang SK, Wang Y, Chen Y, Lou K, Cao LL, Xu LH, Li WJ (2009) Zhihengliuella alba sp. nov., and emended description of the genus Zhihengliuella. Int J Syst Evol Microbiol 59:2025–2031

    Article  CAS  PubMed  Google Scholar 

  • Tseng M, Liao HC, Chiang WP, Yuan GF (2011) Isoptericola chiayiensis sp. nov., isolated from mangrove soil. Int J Syst Evol Microbiol 61:1667–1670

    Article  CAS  PubMed  Google Scholar 

  • Yarza P, Richter M, Peplies J, Euzeby J, Schleifer KH, Ludwig W, Glöckner FO, Rosselló-Móra R (2008) The All-Species Living Tree project: a 16S rRNA-based phylogenetic tree of all sequenced type strains. Syst Appl Microbiol 31:241–250

    Article  CAS  PubMed  Google Scholar 

  • Yoon SH, Ha SM, Kwon S, Lim J, Kim Y, Seo H, Chun J (2017) Introducing EzBioCloud: a taxonomically united database of 16S rRNA and whole genome assemblies. Int J Syst Evol Microbiol 67:1613–1617

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang LY, Fang BZ, Jiao JY, Zhang XT, Liu L, Meng XL, Ming H, Nie GX, Li WJ (2019) Antribacter gilvus gen. nov., sp. nov., a new member of the family from a karstic cavern. Int J Syst Evol Microbiol 69:3792–3799

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

This work was supported by Yunnan Provincial Tea Industry Technical System Construction (Project2017KJTX007) and Yunnan Provincial Key Programs of Yunnan Eco-friendly Food International Cooperation Research Center Project under Grant (Project2019ZG00909-02). We thank Prof. Bernhard Schink and Prof. Aharon Oren for the help of guidance about naming the novel strain.

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Correspondence to Liang Yan, Jie Lv or Jun Sheng.

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The GenBank/EMBL/DDBJ accession numbers for the genome and 16S rRNA gene sequence of TLY-12T are WUWN00000000 and MN014098

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Yang, RJ., Zhou, D., Wang, QM. et al. Puerhibacterium puerhi gen. nov., sp. nov., a novel member of the family Promicromonosporaceae, isolated from Pu-erh tea pile-fermentation. Arch Microbiol 203, 1509–1518 (2021). https://doi.org/10.1007/s00203-020-02151-z

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