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Peteryoungia gen. nov. with four new species combinations and description of Peteryoungia desertarenae sp. nov., and taxonomic revision of the genus Ciceribacter based on phylogenomics of Rhizobiaceae

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Abstract

A novel bacterial strain designated as ADMK78T was isolated from the saline desert soil. The cells were rod-shaped, Gram-stain-negative, and non-motile. The strain ADMK78T grows best at 28 °C. Phylogeny of 16S rRNA gene placed the strain ADMK78T with the members of genera Ciceribacter and Rhizobium, while the highest sequence similarity was with Rhizobium wuzhouense W44T (98.7%) and Rhizobium ipomoeae shin9-1 T (97.9%). Phylogenetic analysis based on 92 core-genes extracted from the genome sequences and average amino acid identity (AAI) revealed that the strain ADMK78T forms a distinct cluster including five species of Rhizobium, which is separate from the cluster of the genera Rhizobium and Ciceribacter. We propose re-classification of Rhizobium ipomoeae, R. wuzhouense, R. rosettiformans and R. rhizophilum into the novel genus Peteryoungia. The average nucleotide identity (ANI) and digital DNA-DNA hybridization (dDDH) values of ADMK78T were less than 82 and 81%, respectively, among all type strains included in the genus Peteryoungia. The strain ADMK78T showed differences in physiological, phenotypic, and protein profiles estimated by MALDI-TOF MS to its closest relatives. Based on the phenotypic, chemotaxonomic properties, and phylogenetic analyses, the strain ADMK78T represents a novel species, Peteryoungia desertarenae sp. nov. The type strain is ADMK78T (= MCC 3400T; KACC 21383T; JCM 33657T). We also proposed the reclassification of Rhizobium daejeonense, R. naphthalenivorans and R. selenitireducens, into the genus Ciceribacter, based on core gene phylogeny and AAI values.

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Data availability

The GenBank accession number for the 16S rRNA gene sequence of strain ADMK78T is MK942856. The draft genome sequence has been deposited in GenBank under the accession number CP058350-CP058352.

References

  • Aliyu H, Lebre P, Blom J, Cowan D, De Maayer P (2016) Phylogenomic re-assessment of the thermophilic genus Geobacillus. Syst Appl Microbiol 39:527–533

    CAS  PubMed  Google Scholar 

  • Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410

    CAS  PubMed  Google Scholar 

  • Aziz RK, Bartels D, Best AA, DeJongh M, Disz T et al (2008) The RAST server: rapid annotations using subsystems technology. BMC Genomics 9:75–15

    PubMed  PubMed Central  Google Scholar 

  • Blin K, Shaw S, Steinke K, Villebro R, Ziemert N, Lee SY, Medema MH, Weber T (2019) AntiSMASH 5.0: updates to the secondary metabolite genome mining pipeline. Nucleic Acid Res 47:W81–W87

    CAS  PubMed  PubMed Central  Google Scholar 

  • Cao J, Wei Y, Lai Q, Wu Y, Deng J, Li J, Liu R, Wang L, Fang J (2020) Georhizobium profundi gen. nov., sp. nov., a piezotolerant bacterium isolated from a deep-sea sediment sample of the New Britain Trench. Int J Syst Evol Microbiol 70:373–379

    CAS  PubMed  Google Scholar 

  • Chaudhari D, Dhotre D, Jani K, Sharma A, Singh Y, Shouche Y, Rahi P (2020) Bacterial communities associated with the biofilms formed in high-altitude brackish water Pangong Tso located in the Himalayan Plateau. Curr Microbiol 77:4072–4084

    PubMed  Google Scholar 

  • Chen C, Chen H, Zhang Y, Thomas HR, Frank MH, He Y, Xia R (2020) TBtools: an integrative toolkit developed for interactive analyses of big biological data. Mol Plant 13(8):1194–1202

    CAS  PubMed  Google Scholar 

  • Chun J, Oren A, Ventosa A, Christensen H, Arahal DR et al (2018) Proposed minimal standards for the use of genome data for the taxonomy of prokaryotes. Int J Syst Evol Microbio 68:461–466

    CAS  Google Scholar 

  • Conn HJ (1938) Agricultural and industrial bacteriology. J Bacteriol 36:320–321

    Google Scholar 

  • Efron B, Halloran E, Holmes S (1996) Bootstrap confidence levels for phylogenetic trees. Proc Natl Acad Sci USA 93(23):13429

    CAS  PubMed  PubMed Central  Google Scholar 

  • Espariz M, Zuljan FA, Esteban L, Magni C (2016) Taxonomic identity resolution of highly phylogenetically related strains and selection of phylogenetic markers by using genome-scale methods: the Bacillus pumilus group case. PLoS ONE 11:e0163098

    PubMed  PubMed Central  Google Scholar 

  • Frank B (1889) Über die Pilzsymbiose der Leguminosen. Ber Dtsch Bot Ges 7:332–346 (in German)

    Google Scholar 

  • Gao JL, Wang LW, Xue J, Tong S, Peng G, Sun YC, Zhang X, Sun J-G (2020) Rhizobium rhizophilum sp. nov., an indole acetic acid-producing bacterium isolated from rape (Brassica napus L.) rhizosphere soil. Int J Syst Evol Microbio 70:5019–5025

    CAS  Google Scholar 

  • Gulati A, Rahi P, Vyas P (2008) Characterization of phosphate-solubilizing fluorescent pseudomonads from the rhizosphere of seabuckthorn growing in the cold deserts of Himalayas. Curr Microbiol 56:73–79

    CAS  PubMed  Google Scholar 

  • He X, Chang W, Pierce DL, Seib LO, Wagner J, Fuqua C (2003) Quorum sensing in Rhizobium sp. strain NGR234 regulates conjugal transfer (tra) gene expression and influences growth rate. J Bacteriol 185(3):809–822

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hördt A, López MG, Meier-Kolthoff JP, Schleuning M, Weinhold L-M, Tindall BJ, Gronow S, Kyrpides NC, Woyke T, Göker M (2020) Analysis of 1000+ type-strain genomes substantially improves taxonomic classification of Alphaproteobacteria. Front Microbiol 11:468

    PubMed  PubMed Central  Google Scholar 

  • Hunter WJ, Kuykendall LD, Manter DK (2007) Rhizobium selenireducens sp. nov.: a selenite-reducing alpha-Proteobacteria isolated from a bioreactor. Curr Microbiol 55:455–460

    CAS  PubMed  Google Scholar 

  • Jain C, Rodriguez-R LM, Phillippy AM, Konstantinidis KT, Aluru S (2018) High throughput ANI analysis of Meier-Kolthoff 90K prokaryotic genomes reveals clear species boundaries. Nat Commun 9:5114

    PubMed  PubMed Central  Google Scholar 

  • Kaiya S, Rubaba O, Yoshida N, Yamada T, Hiraishi A (2012) Characterization of Rhizobium naphthalenivorans sp. nov. with special emphasis on aromatic compound degradation and multilocus sequence analysis of housekeeping genes. J Gen Appl Microbiol 58:211–224

    CAS  PubMed  Google Scholar 

  • Kathiravan R, Jegan S, Ganga V, Prabavathy VR, Tushar L, Sasikala Ch, Ramana ChV (2013) Ciceribacter lividus gen. nov., sp. nov., isolated from rhizosphere soil of chick pea (Cicer arietinum L.). Int J Syst Evol Microbiol 63:4484–4488

    CAS  PubMed  Google Scholar 

  • Kaur J, Verma M, Lal R (2011) Rhizobium rosettiformans sp. nov., isolated from a hexachlorocyclohexane dump site, and reclassification of Blastobacter aggregatus Hirsch and Muller 1986 as Rhizobium aggregatum comb. nov. Int J Syst Evol Microbiol 61:1218–1225

    CAS  PubMed  Google Scholar 

  • Kimes NE, Lopez-Perez M, Flores-Felix JD, Ramirez-Bahena MH, Igual JM, Peix A, Rodriguez-Valera F, Velazquez E (2015) Pseudorhizobium pelagicum gen. nov., sp. nov. isolated from a pelagic Mediterranean zone. Syst Appl Microbiol 38:293–299

    PubMed  Google Scholar 

  • Koren S, Walenz BP, Berlin K, Miller JR, Bergman NH et al (2017) Canu: scalable and accurate long-read assembly via adaptive k-mer weighting and repeat separation. Genome Res 27:722–736

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kurli R, Chaudhari D, Pansare AN, Khairnar M, Shouche YS, Rahi P (2018) Cultivable microbial diversity associated with cellular phones. Front Microbiol 9:1229

    PubMed  PubMed Central  Google Scholar 

  • Kurtz S, Phillippy A, Delcher AL, Smoot M, Shumway M et al (2004) Versatile and open software for comparing large genomes. Genome Biol 5(2):R12

    PubMed  PubMed Central  Google Scholar 

  • Kuykendall LD (2005) Rhizobiales ord. nov. In Bergey's Manual of Systematic Bacteriology, 2nd edn, vol. 2 (The Proteobacteria), part C (The Alpha-, Beta-, Delta-, and Epsilonproteobacteria), pp. 324–361. Edited by Brenner DJ, Krieg NR, Staley JT, Garrity GM, Springer, New York.

  • Langmead B, Salzberg SL (2012) Fast gapped-read alignment with Bowtie 2. Nat Methods 9:357–359

    CAS  PubMed  PubMed Central  Google Scholar 

  • Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and clustal X version 2.0. Bioinformatics 23:2947–2948

    CAS  PubMed  Google Scholar 

  • Letunic I, Bork P (2019) Interactive Tree Of Life (iTOL) v4: recent updates and new developments. Nucleic Acids Res 47:W256–W259

    CAS  PubMed  PubMed Central  Google Scholar 

  • Li Y, Lei X, Xu Y, Zhu H, Xu M et al (2017) Rhizobium albus sp. nov., isolated from lake water in Xiamen Fujian Province of China. Curr Microbiol 74:42–48

    CAS  PubMed  Google Scholar 

  • Li Y, Xue H, Sang SQ, Lin CL, Wang XZ (2017) Phylogenetic analysis of family Neisseriaceae based on genome sequences and description of Populibacter corticis gen nov, sp nov, a member of the family Neisseriaceae, isolated from symptomatic bark of Populus x euramericana canker. PLoS One 12:e0174506

    PubMed  PubMed Central  Google Scholar 

  • Lindström K, Mousavi SA (2010) Rhizobium and other N-fixing symbioses. In: Encyclopedia of Life Science (ELS). Chichester: John Wiley and Sons.

  • Lindström K, Amsalu AA, Mousavi SA (2015) Evolution and taxonomy of nitrogen-fixing organisms with emphasis on rhizobia. In: de Bruijn FJ (ed) Biological nitrogen fixation. Wiley, Hoboken, NJ, pp 21–38

    Google Scholar 

  • Lopes-Santos L, Castro DBA, Ferreira-Tonin M, Correa DBA, Weir BS et al (2017) Reassessment of the taxonomic position of Burkholderia andropogonis and description of Robbsia andropogonis gen. nov., comb. nov. Antonie Van Leeuwenhoek 110:727–736

    CAS  PubMed  Google Scholar 

  • Luo C, Rodriguez-R LM, Konstantinidis KT (2014) MyTaxa: an advanced taxonomic classifier for genomic and metagenomic sequences. Nucleic Acids Res 42(8):e73

    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 Bioinformat 14:60

    Google Scholar 

  • Minas K, McEwan NR, Newbold CJ, Scott KP (2011) Optimization of a high-throughput CTAB-based protocol for the extraction of qPCR-grade DNA from rumen fluid, plant and bacterial pure cultures. FEMS Microbiol Lett 325(2):162–169. https://doi.org/10.1111/j.1574-6968.2011.02424.x

    Article  CAS  PubMed  Google Scholar 

  • Mohapatra B, Sarkar A, Joshi S, Chatterjee A, Kazy SK et al (2017) An arsenate-reducing and alkane-metabolizing novel bacterium, Rhizobium arsenicireducens sp. nov., isolated from arsenic-rich groundwater. Arch Microbiol 199:191–201

    CAS  PubMed  Google Scholar 

  • Mousavi SA, Osterman J, Wahlberg N, Nesme X, Lavire C, Vial L, Paulin L, de Lajudie P, Lindstrom K (2014) Phylogeny of the Rhizobium-Allorhizobium-Agrobacterium clade supports the delineation of Neorhizobium gen. nov. Syst Appl Microbiol 37:208–215

    CAS  PubMed  Google Scholar 

  • Mousavi SA, Willems A, Nesme X, de Lajudie P, Lindstrom K (2015) Revised phylogeny of Rhizobiaceae: proposal of the delineation of Pararhizobium gen. nov., and 13 new species combinations. Syst Appl Microbiol 38:84–90

    PubMed  Google Scholar 

  • Na SI, Kim YO, Yoon S-H, Ha S, Baek I et al (2018) UBCG: up-to-date bacterial core gene set and pipeline for phylogenomic tree reconstruction. J Microbiol 56:280–285

    CAS  PubMed  Google Scholar 

  • Oresnik IJ, Twelker S, Hynes MF (1999) Cloning and characterization of a Rhizobium leguminosarum gene encoding a bacteriocin with similarities to RTX toxins. Appl Environ Microbiol 65(7):2833–2840

    CAS  PubMed  PubMed Central  Google Scholar 

  • Panday D, Schumann P, Das SK (2011) Rhizobium pusense sp. nov., isolated from the rhizosphere of chickpea (Cicer arietinum L.). Int J Syst Evol Microbiol 61:2632–2639

    PubMed  Google Scholar 

  • Pandit AS, Joshi MN, Bhargava P, Shaikh I, Ayachit GN et al (2015) A snapshot of microbial communities from the Kutch: one of the largest salt deserts in the World. Extremophiles 19:973–987

    PubMed  Google Scholar 

  • Park S, Lee JS, Lee KC, Yoon JH (2013) Lentilitoribacter donghaensis gen. nov., sp. nov., a slowly-growing alphaproteobacterium isolated from coastal seawater. Antonie Van Leeuwenhoek 103:457–464

    PubMed  Google Scholar 

  • Parks DH, Chuvochina M, Chaumeil PA, Rinke C, Mussig AJ, Hugenholtz P (2020) A complete domain-to-species taxonomy for Bacteria and Archaea. Nat Biotechnol 38:1079–1086

    CAS  PubMed  Google Scholar 

  • Parte AC, Sardà Carbasse J, 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

    PubMed  PubMed Central  Google Scholar 

  • Peix A, Rivas R, Trujillo ME, Vancanneyt M, Velazquez E, Willems A (2005) Reclassification of Agrobacterium ferrugineum LMG 128 as Hoeflea marina gen. nov., sp. nov. Int J Syst Evol Microbiol 55:1163–1166

    CAS  PubMed  Google Scholar 

  • 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(12):2210–2215

    PubMed  PubMed Central  Google Scholar 

  • Quan ZX, Bae HS, Baek JH, Chen WF, Im WT et al (2005) Rhizobium daejeonense sp. nov. isolated from a cyanide treatment bioreactor. Int J Syst Evol Microbiol 55:2543–2549

    CAS  PubMed  Google Scholar 

  • Rahi P, Kurli R, Khairnar M, Jagtap S, Pansare AN et al (2017) Description of Lysinibacillus telephonicus sp. nov., isolated from the screen of a cellular phone. Int J Syst Evol Microbiol 67:2289–2295

    CAS  PubMed  Google Scholar 

  • Ramana CV, Parag B, Girija KR, Raghu Ram B, Venkata Ramana V et al (2013) Rhizobium subbaraonis sp. nov., an endolithic bacterium isolated from beach sand. Int J Syst Evol Microbiol 63:581–585

    CAS  PubMed  Google Scholar 

  • Rivas R, Sanchez-Marquez S, Mateos PF, Martinez-Molina E, Velazquez E (2005) Martelella mediterranea gen. nov., sp. nov., a novel alpha-proteobacterium isolated from a subterranean saline lake. Int J Syst Evol Microbiol 55:955–959

    CAS  PubMed  Google Scholar 

  • Ruginescu R, Gomoiu I, Popescu O, Cojoc R, Neagu S, Lucaci I, Batrinescu-Moteau C, Enache M (2020) Bioprospecting for novel halophilic and halotolerant sources of hydrolytic enzymes in brackish, saline and hypersaline lakes of Romania. Microorganisms. 8(12):1903.

  • Sasser M (2001) Technical note # 101 identification of bacteria by gas chromatography of cellular fatty acids. Stat:1–6.

  • Sheu SY, Chen ZH, Young CC, Chen WM (2016) Rhizobium ipomoeae sp. nov., isolated from a water convolvulus field. Int J Syst Evol Microbiol 66:1633–1640

    CAS  PubMed  Google Scholar 

  • Stamatakis A (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30:1312–1313

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tittsler RP, Sandholzer LA (1936) The use of semi-solid agar for the detection of bacterial motility. J Bacteriol 31:575–580

    CAS  PubMed  PubMed Central  Google Scholar 

  • Walker BJ, Abeel T, Shea T, Priest M, Abouelliel A et al (2014) Pilon: an integrated tool for comprehensive microbial variant detection and genome assembly improvement. PLoS One 9:e112963. https://doi.org/10.1371/journal.pone.0112963

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang Q, Zhu W, Wang ET, Zhang LS, Li X et al (2016) Genomic identification of rhizobia-related strains and threshold of ANI and core-genome for family, genus and species. Int J Environ Agri Res 2:76–86

    Google Scholar 

  • Wang C, Li A, Yuan T, Bao G, Feng G, Zhu H (2020) Rhizobium glycinendophyticum sp. nov., isolated from roots of Glycine max (Linn. Merr.). Antonie Van Leeuwenhoek 113:147–154

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Yoon S-H, Ha S-M, Kwon S, Lim J, Kim Y et al (2017) Introducing EzBioCloud: a taxonomically United database of 16S rRNA gene sequences and whole-genome assemblies. Int J Syst Evol Microbiol 67:1613–1617

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yuan T, Liu L, Huang S, Taher AH, Tan Z et al (2018) Rhizobium wuzhouense sp. nov., isolated from roots of Oryza officinalis. Int J Syst Evol Microbiol 68:2918–2923

    CAS  PubMed  Google Scholar 

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Acknowledgements

The authors thank Prof. Aharon Oren, Department of Plant and Environmental Sciences, The Hebrew University of Jerusalem, Israel, and Prof. Bernhard Schink, Department of Biology, University of Konstanz, Germany, for their expert suggestions concerning the correct species name, species epithet and Latin etymology. Authors also thank Prof J Peter W Young, University of York, to grant us permission to propose new genus Peteryoungia. The authors acknowledge the financial support of the Department of Biotechnology (BT/Coord. II/01/03/2016).

Funding

Financial support by the Department of Biotechnology (BT/Coord. II/01/03/2016) and (BT/PR8218/BCE/8/1044/2013).

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Authors and Affiliations

  1. National Centre for Microbial Resource, National Centre for Cell Science, Pune, Maharashtra, 411007, India

    Praveen Rahi, Mitesh Khairnar, Ashwini Hagir, Aabeejjeet Pansare & Yogesh Shouche

  2. Post-Graduate Department of Biosciences, UGC-Centre of Advanced Study, Sardar Patel University, Satellite Campus, Vadtal Road, Bakrol, Anand, Gujarat, 388 315, India

    Avinash Narayan, Kunal R. Jain & Datta Madamwar

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  1. Praveen Rahi
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Contributions

MK: methodology, formal analysis, validation; AH and AP: methodology, formal analysis; AN and KJ methodology, isolation; DM and YS funding acquisition; PR conceptualization, methodology, data curation, formal analysis, supervision, and writing.

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Correspondence to Praveen Rahi.

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Rahi, P., Khairnar, M., Hagir, A. et al. Peteryoungia gen. nov. with four new species combinations and description of Peteryoungia desertarenae sp. nov., and taxonomic revision of the genus Ciceribacter based on phylogenomics of Rhizobiaceae. Arch Microbiol 203, 3591–3604 (2021). https://doi.org/10.1007/s00203-021-02349-9

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