Mesorhizobium composti sp. nov., isolated from compost

Abstract

A polyphasic taxonomic approach was used to characterize a presumptively novel diazotrophic bacterium, designated strain CC-YTH430T, isolated from a compost sample in Taiwan. Cells of strain CC-YTH430T were found to be Gram-stain negative, facultative anaerobic rods that formed yellow-colored colonies on nutrient agar. Cell growth occurred at 15–40 °C, pH 5.0–9.0 and in the presence of 0–2% NaCl. Strain CC-YTH430T resembled Mesorhizobium species while sharing high pair-wise 16S rRNA gene sequence similarities with Mesorhizobium silamurunense, Mesorhizobium thiogangeticum, Mesorhizobium plurifarium, Mesorhizobium tamadayense, Mesorhizobium amorphae (96.9% each), Mesorhizobium sediminum (96.8%), and Mesorhizobium soli (96.5%) and < 96.5% similarity to other species. Strain CC-YTH430T showed 78.8–79.7% average nucleotide identity compared to the type strains of M. amorphae, M. plurifarium, M. soli, M. tamadayense and M. wenxiniae. The N2-fixing activity of strain CC-YTH430T was 0.2 nmol ethylene h−1 at 30 °C. The respiratory system was ubiquinone 10 (Q-10) and the DNA G+C content was 62.0 ± 0.2 mol%. The major fatty acids (> 5%) were C16:0, C17:0 cyclo, C19:0 cyclo ω8c, C14:0 3OH/C16:1 iso I and C18:1ω7c/C18:1ω6c. The polar lipid profile contained diphosphatidylglycerol, phosphatidylglycerol, phosphatidylcholine, phosphatidylmonomethylethanolamine and an unidentified aminolipid in major amounts. In addition, phosphatidylethanolamine, an unidentified lipid and several unidentified polar lipids were also found in moderate-to-trace amounts. Based on the phylogenetic, phenotypic and chemotaxonomic features, strain CC-YTH430T is proposed to represent a novel Mesorhizobium species, for which the name Mesorhizobium composti sp. nov. (type strain CC-YTH430T = BCRC 81024T = JCM 31762T) is proposed.

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Abbreviations

AL1–2:

Unidentified aminolipids

ANI:

Average nucleotide identity

APL:

Unidentified aminophospholipid

BCRC:

Bioresource Collection and Research Center

DPG:

Diphosphatidylglycerol

DSMZ:

Deutsche Sammlung von Mikroorganismen und Zellkulturen

FAME:

Fatty acid methyl esters

FID:

Flame-ionization detector

HPLC:

High-performance liquid chromatography

JCM:

Japan Collection of Microorganisms

KCTC:

Korean Collection for Type Cultures

L1:

Unidentified lipid

MA:

Marine agar

MIDI:

Microbial identification

NA:

Nutrient agar

NB:

Nutrient broth

PC:

Phosphatidylcholine

PE:

Phosphatidylethanolamine

PG:

Phosphatidylglycerol

PL1–6:

Unidentified phospholipids

PME:

Phosphatidylmonomethylethanolamine

tr:

Trace

TSA:

Tryptic soy agar

YMA:

Yeast extract mannitol agar

References

  1. Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M, Kulikov AS, Lesin VM, Nikoleko 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 

  2. Bernardet JF, Nakagawa Y, Holmes B (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

    CAS  Google Scholar 

  3. Chen WX, Wang ET, Kuykendall LD (2005) Genus VI. Mesorhizobium Jarvis, van Berkum, Chen, Nour, Fernandez, Cleyet-Marel and Gillis 1997, 897VP. In: Brenner DJ, Krieg NR, Staley JT, Garrity GM (eds) Bergey’s manual of systematic bacteriology, vol 2, part C, 2nd edn. Springer, New York, pp 403–408

    Google Scholar 

  4. Chun J, Oren A, Ventosa A, Christensen H, Arahal DR, da Costa MS, Rooney AP, Yi H, Xu XW, Meyer SD, Trujillo ME (2018) Proposed minimal standards for the use of genome data for the taxonomy of prokaryotes. Int J Syst Evol Microbiol 68:461–466

    Article  PubMed  Google Scholar 

  5. Clarke PH, Cowan ST (1952) Biochemical methods for bacteriology. J Gen Microbiol 6:187

    Article  CAS  PubMed  Google Scholar 

  6. Collins MD (1985) Isoprenoid quinone analysis in classification and identification. In: Goodfellow M, Minnikin DE (eds) Chemical methods in bacterial systematics. Academic Press, London, pp 267–287

    Google Scholar 

  7. de Lajudie P, Willems A, Nick G, Moreira F, Molouba F, Hoste B, Torck U, Neyra M, Collins MD, Lindstrőm K, Dreyfus B, Gillis M (1998) Characterization of tropical tree rhizobia and description of Mesorhizobium plurifarium sp. nov. Int J Syst Bacteriol 48:369–382

    Article  PubMed  Google Scholar 

  8. Felsenstein J (1981) Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol 17:368–376

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

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

    Article  Google Scholar 

  11. Gaunt MW, Turner SL, Rigottier-Gois L, Lloyd-Macgilp SA, Young JPW (2001) Phylogenies of atpD and recA support the small subunit rRNA-based classification of rhizobia. Int J Syst Evol Microbiol 51:2037–2048

    Article  CAS  PubMed  Google Scholar 

  12. Ghosh W, Roy P (2006) Mesorhizobium thiogangeticum sp. nov., a novel sulfur-oxidizing chemolithoautotroph from rhizosphere soil of an Indian tropical leguminous plant. Int J Syst Evol Microbiol 56:91–97

    Article  CAS  PubMed  Google Scholar 

  13. Hameed A, Shahina M, Lai WA, Lin SY, Young LS, Liu YC, Hsu YH, Young CC (2015) Oricola cellulosilytica gen. nov., sp nov., a cellulose-degrading bacterium of the family Phyllobacteriaceae isolated from surface seashore water, and emended descriptions of Mesorhizobium loti and Phyllobacterium myrsinacearum. Antonie Van Leeuwenhoek 107:759–771

    Article  CAS  PubMed  Google Scholar 

  14. Hardy R, Burns RC, Holsten RD (1973) Application of the acetylene–ethylene assay for measurement of nitrogen fixation. Soil Biol Biochem 5:47–81

    Article  CAS  Google Scholar 

  15. Heiner CR, Hunkapiller LK, Chen SM, Glass JI, Chen EY (1998) Sequencing multimegabase-template DNA using BigDye terminator chemistry. Genome Res 8:557–561

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Jarvis BDW, Pankhurst CE, Patel JJ (1982) Rhizobiurn loti, a new species of legume root nodule bacteria. Int J Syst Bacteriol 32:378–380

    Article  Google Scholar 

  17. Jarvis BDW, Van Berkum P, Chen WX, Nour SM, Fernandez MP, Cleyet-Marel JC, Gillis M (1997) Transfer of Rhizobium loti, Rhizobium huakuii, Rhizobium ciceri, Rhizobium mediterraneum, and Rhizobium tianshanense to Mesorhizobium gen. nov. Int J Syst Bacteriol 47:895–898

    Article  Google Scholar 

  18. Jukes TH, Cantor CR (1969) Evolution of protein molecules. In: Munro HN (ed) Mammalian protein metabolism. Academic Press, New York, pp 21–32

    Google Scholar 

  19. Koch B, Evans HJ (1966) Reduction of acetylene to ethylene by soybean root nodules. Plant Physiol 41:1748–1750

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Kuklinsky-Sobral J, Araujo WL, Mendes R, Geraldi IO, Pizzirani-Kleiner AA, Azevedo JL (2004) Isolation and characterization of soybean-associated bacteria and their potential for plant growth promotion. Environ Microbiol 6:1244–1251

    Article  CAS  PubMed  Google Scholar 

  21. Laguerre G, Nour SM, Macheret V, Sanjuan J, Drouin P, Amarger N (2001) Classification of rhizobia based on nodC and nifH gene analysis reveals a close phylogenetic relationship among Phaseolus vulgaris symbionts. Microbiology 147:981–993

    Article  CAS  PubMed  Google Scholar 

  22. Laranjo M, Alexandre A, Oliveira S (2014) Legume growthpromoting rhizobia: an overview on the Mesorhizobium genus. Microbiol Res 169:2–17

    Article  PubMed  Google Scholar 

  23. Lee I, Ouk Kim Y, Park SC, Chun J (2016) OrthoANI: an improved algorithm and software for calculating average nucleotide identity. Int J Syst Evol Microbiol 66:1100–1103

    Article  CAS  Google Scholar 

  24. Marcos-García M, Menéndez E, Ramírez-Bahena MH, Mateos PF, Peix Á, Velazquez E, Rivas R (2017) Mesorhizobium helmanticense sp. nov., isolated from Lotus corniculatus nodules. Int J Syst Evol Microbiol 67:2301–2305

    Article  CAS  PubMed  Google Scholar 

  25. Mesbah M, Premachandran U, Whitman WB (1989) Precise measurement of the G+C content of deoxyribonucleic acid by high performance liquid chromatography. Int J Syst Bacteriol 39:159–167

    Article  CAS  Google Scholar 

  26. Meyer SED, Tan HW, Andrews M, Heenan PB, Willems A (2016) Mesorhizobium calcicola sp. nov., Mesorhizobium waitakense sp. nov., Mesorhizobium sophorae sp. nov., Mesorhizobium newzealandense sp. nov. and Mesorhizobium kowhaii sp. nov. isolated from Sophora root nodules. Int J Syst Evol Microbiol 66:786–795

    Article  CAS  PubMed  Google Scholar 

  27. Miller LT (1982) Single derivatization method for routine analysis of bacterial whole-cell fatty acid methyl esters, including hydroxyl acids. J Clin Microbiol 16:584–586

    CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  Google Scholar 

  29. Murray RGE, Doetsch RN, Robinow CF (1994) Determination 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, pp 32–34

    Google Scholar 

  30. Paisley R (1996) MIS whole cell fatty acid analysis by gas chromatography training manual. MIDI, Newark

    Google Scholar 

  31. Poly F, Monrozier LJ, Bally R (2001) Improvement in the RFLP procedure for studying the diversity of nifH genes in communities of nitrogen fixers in soil. Res Microbiol 152:95–103

    Article  CAS  PubMed  Google Scholar 

  32. Ramírez-Bahena MH, Hernández M, Peix Á, Velázquez E, León-Barrios M (2012) Mesorhizobial strains nodulating Anagyris latifolia and Lotus berthelotii in Tamadaya ravine (Tenerife, Canary Islands) are two symbiovars of the same species, Mesorhizobium tamadayense sp. nov. Syst Appl Microbiol 35:334–341

    Article  PubMed  Google Scholar 

  33. 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  Google Scholar 

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

    CAS  Google Scholar 

  35. Sarita S, Sharma PK, Priefer UB, Prell J (2005) Direct amplification of rhizobial nodC sequences from soil total DNA and comparison to nodC diversity of root nodule isolates. FEMS Microbiol Ecol 54:1–11

    Article  CAS  PubMed  Google Scholar 

  36. Sasser M (1990) Identification of bacteria by gas chromatography of cellular fatty acids, MIDI technical note 101. MIDI Inc, Newark

    Google Scholar 

  37. Stackebrandt E, Goebel BM (1994) Taxonomic note: a place for DNA-DNA reassociation and 16S rRNA sequence analysis in the present species definition in bacteriology. Int J Syst Bacteriol 44:846–849

    Article  CAS  Google Scholar 

  38. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Vincent JM (1970a) A manual for the practical study of root-nodule bacteria. Blackwell Scientific, Oxford

    Google Scholar 

  41. Vincent JM (1970b) The cultivation, isolation and maintenance of rhizobia. In: Vincent JM (ed) A manual for the practical study of the root-nodule bacteria. Blackwell Scientific, Oxford, pp 1–13

    Google Scholar 

  42. Xie CH, Yokota A (2004) Phylogenetic analyses of the nitrogen-fixing genus Derxia. J Gen Appl Microbiol 50:129–135

    Article  CAS  PubMed  Google Scholar 

  43. 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 

  44. Yuan CG, Jiang Z, Xizo M, Zhou EM, Kim CJ, Hozzein WN, Park DJ, Zhi XY, Li WJ (2016) Mesorhizobium sediminum sp. nov., isolated from deep-sea sediment. Int J Syst Evol Microbiol 11:4797–4802

    Google Scholar 

  45. Zehr JP, McReynolds LA (1989) Use of degenerate oligonucleotides for amplification of the nifH gene from the marine cyanobacterium Trichodesmium thiebautii. Appl Environ Microbiol 55:2522–2526

    CAS  PubMed  PubMed Central  Google Scholar 

  46. Zehr JP, Jenkins BD, Short SM, Steward GF (2003) Nitrogenase gene diversity and microbial community structure: a crosssystem comparison. Environ Microbiol 5:539–554

    Article  CAS  PubMed  Google Scholar 

  47. Zhao CT, Wang ET, Zhang YM, Chen WF, Sui XH, Chen WX, Liu HC, Zhang XX (2012) Mesorhizobium silamurunense sp. nov., isolated from root nodules of Astragalus species. Int J Syst Evol Microbiol 62:21803–22186

    Google Scholar 

  48. Zhou J, Fries MR, Chee-Sanford JC, Tiedje JM (1995) Phylogenetic analyses of a new group of denitrifiers capable of anaerobic growth of toluene and description of Azoarcus tolulyticus sp. nov. Int J Syst Bacteriol 45:500–506

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

This work was financially supported by the Ministry of Science and Technology (Taiwan) under Grant No. MOST 107-2634-F-005-002 and by the “Innovation and Development Center of Sustainable Agriculture” from The Featured Areas Research Center Program within the framework of the Higher Education Sprout Project by the Ministry of Education (MOE) in Taiwan.

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SYL analyzed most of the data and wrote the manuscript. AH contributed to providing critical revisions to this article. YTH was responsible for collecting samples and isolating the novel microorganism. All authors discussed the results and revised the manuscript.

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Correspondence to Chiu-Chung Young.

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The GenBank/EMBL/DDBJ accession numbers for the 16S rRNA, atpD, recA gene sequences and the draft genome of Mesorhizobium composti strain CC-YTH430T are KX988315, MG708501, MG708502 and SSNY00000000, respectively.

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Lin, SY., Hameed, A., Hsieh, YT. et al. Mesorhizobium composti sp. nov., isolated from compost. Antonie van Leeuwenhoek 112, 1387–1398 (2019). https://doi.org/10.1007/s10482-019-01270-y

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Keywords

  • Mesorhizobium composti
  • Phyllobacteriaceae
  • Polyphasic taxonomy
  • Compost