1887

INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY logo

Volume 74, Issue 2

Three Fe(III)-reducing and nitrogen-fixing bacteria, sp. nov., sp. nov. and sp. nov., isolated from paddy soil No Access

Abstract

Three microaerophilic bacterial strains, designated SG22, SG63 and SG29 were isolated from paddy soils in PR China. Cells of these strains were Gram-staining-negative and long rod-shaped. SG22, SG63 and SG29 showed the highest 16S rRNA gene sequence similarities with the members of the genus . The results of phylogenetic and phylogenomic analysis also indicated that these strains clustered with members of the genus . The main respiratory menaquinone of SG22, SG63 and SG29 was MK-8 and the major fatty acids were iso-C, iso-C and C. SG22, SG29 and SG63 not only possessed iron reduction ability but also harboured genes () encoding nitrogenase. The genomic DNA G+C contents of SG22, SG63 and SG29 ranged from 73.3 to 73.5 %. The average nucleotide identity (ANI) and digital DNA–DNA hybridisation (dDDH) values between SG22, SG63 and SG29 and the closely related species of the genus were lower than the cut-off values (dDDH 70 % and ANI 95–96 %) for prokaryotic species delineation. On the basis of these results, strains SG22, SG63 and SG29 represent three novel species within the genus , for which the names sp. nov., sp. nov. and sp. nov., are proposed. The type strains are SG22 (= GDMCC 1.3185 = JCM 35581), SG63 (= GDMCC 1.2914 = JCM 35124) and SG29 (= GDMCC 1.2911 = JCM 35123).

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): Anaeromyxobacter oryzisoli , Anaeromyxobacter soli , Anaeromyxobacter terrae , Novel species and paddy soil
Funding
This study was supported by the:
  • Key project of science and Technology innovation in Fujian Province, China (Award 2022G02014)
    • Principle Award Recipient: LiuGuo-Hong
  • National Natural Science Foundation of China (Award 42177270)
    • Principle Award Recipient: YongYuan
  • Key Technology Research and Development Program of Shandong (Award 2021YFD1900400)
    • Principle Award Recipient: Qiu-EYang
© 2024 The Authors
Loading

Article metrics loading...

/content/journal/ijsem/10.1099/ijsem.0.006268
2024-02-07
2024-05-20
Loading full text...

Full text loading...

References

  1. Ishii S, Ikeda S, Minamisawa K, Senoo K. Nitrogen cycling in rice paddy environments: past achievements and future challenges. Microbes Environ 2011; 26:282–292 [View Article] [PubMed]
     [Google Scholar]
  2. Masuda Y, Shiratori Y, Ohba H, Ishida T, Takano R et al. Enhancement of the nitrogen-fixing activity of paddy soils owing to iron application. Soil Sci Plant Nutr 2021; 67:243–247 [View Article]
     [Google Scholar]
  3. Masuda Y, Yamanaka H, Xu ZX, Shiratori Y, Aono T et al. Diazotrophic Anaeromyxobacter isolates from soils. Appl Environ Microbiol 2020; 86:e00956-20 [View Article]
     [Google Scholar]
  4. Onley JR, Ahsan S, Sanford RA, Löffler FE, Drake HL. Denitrification by Anaeromyxobacter dehalogenans, a common soil bacterium lacking the nitrite reductase genes nirS and nirK. Appl Environ Microbiol 2018; 84:e01985-17 [View Article] [PubMed]
     [Google Scholar]
  5. Sanford RA, Wagner DD, Wu Q, Chee-Sanford JC, Thomas SH et al. Unexpected nondenitrifier nitrous oxide reductase gene diversity and abundance in soils. Proc Natl Acad Sci U S A 2012; 109:19709–19714 [View Article] [PubMed]
     [Google Scholar]
  6. Sanford RA, Cole JR, Tiedje JM. Characterization and description of Anaeromyxobacter dehalogenans gen. nov., sp. nov., an aryl-halorespiring facultative anaerobic myxobacterium. Appl Environ Microbiol 2002; 68:893–900 [View Article] [PubMed]
     [Google Scholar]
  7. Itoh H, Xu Z, Mise K, Masuda Y, Ushijima N et al. Anaeromyxobacter oryzae sp. nov., Anaeromyxobacter diazotrophicus sp. nov. and Anaeromyxobacter paludicola sp. nov., isolated from paddy soils. Int J Syst Evol Microbiol 2022; 72:5546 [View Article]
     [Google Scholar]
  8. Treude N, Rosencrantz D, Liesack W, Schnell S. Strain FAc12, a dissimilatory iron-reducing member of the Anaeromyxobacter subgroup of Myxococcales. FEMS Microbiol Ecol 2003; 44:261–269 [View Article] [PubMed]
     [Google Scholar]
  9. Kudo K, Yamaguchi N, Makino T, Ohtsuka T, Kimura K et al. Release of arsenic from soil by a novel dissimilatory arsenate-reducing bacterium, Anaeromyxobacter sp. strain PSR-1. Appl Environ Microbiol 2013; 79:4635–4642 [View Article] [PubMed]
     [Google Scholar]
  10. Wu Q, Sanford RA, Löffler FE. Uranium(VI) reduction by Anaeromyxobacter dehalogenans strain 2CP-C. Appl Environ Microbiol 2006; 72:3608–3614 [View Article] [PubMed]
     [Google Scholar]
  11. Strycharz SM, Gannon SM, Boles AR, Franks AE, Nevin KP et al. Reductive dechlorination of 2-chlorophenol by Anaeromyxobacter dehalogenans with an electrode serving as the electron donor. Environ Microbiol Rep 2010; 2:289–294 [View Article] [PubMed]
     [Google Scholar]
  12. Thomas SH, Wagner RD, Arakaki AK, Skolnick J, Kirby JR et al. The mosaic genome of Anaeromyxobacter dehalogenans strain 2CP-C suggests an aerobic common ancestor to the delta-proteobacteria. PLoS One 2008; 3:e2103 [View Article] [PubMed]
     [Google Scholar]
  13. Cole JR, Cascarelli AL, Mohn WW, Tiedje JM. Isolation and characterization of a novel bacterium growing via reductive dehalogenation of 2-chlorophenol. Appl Environ Microbiol 1994; 60:3536–3542 [View Article] [PubMed]
     [Google Scholar]
  14. Hwang C, Copeland A, Lucas S, Lapidus A, Barry K et al. Complete genome sequence of Anaeromyxobacter sp. Fw109-5, an anaerobic, metal-reducing bacterium isolated from a contaminated subsurface environment. Genome Announc 2015; 3:e01449-14 [View Article] [PubMed]
     [Google Scholar]
  15. Masuda Y, Itoh H, Shiratori Y, Isobe K, Otsuka S et al. Predominant but previously-overlooked prokaryotic drivers of reductive nitrogen transformation in paddy soils, revealed by metatranscriptomics. Microbes Environ 2017; 32:180–183 [View Article] [PubMed]
     [Google Scholar]
  16. Parte AC, Sardà Carbasse J, Meier-Kolthoff JP, Reimer LC, Göker M. List of Prokaryotic names with Standing in Nomenclature (LPSN) moves to the DSMZ. Int J Syst Evol Microbiol 2020; 70:5607–5612 [View Article] [PubMed]
     [Google Scholar]
  17. Liu GH, Yang S, Tang R, Xie CJ, Zhou SG. Genome analysis and description of three novel diazotrophs Geomonas species isolated from paddy soils. Front Microbiol 2021; 12:801462 [View Article] [PubMed]
     [Google Scholar]
  18. Li J, Liu P, Menguy N, Benzerara K, Bai J et al. Identification of sulfate-reducing magnetotactic bacteria via a group-specific 16S rDNA primer and correlative fluorescence and electron microscopy: strategy for culture-independent study. Environ Microbiol 2022; 24:5019–5038 [View Article] [PubMed]
     [Google Scholar]
  19. Yoon S-H, Ha S-M, Kwon S, Lim J, Kim Y et al. Introducing EzBioCloud: a taxonomically united database of 16S rRNA gene sequences and whole-genome assemblies. Int J Syst Evol Microbiol 2017; 67:1613–1617 [View Article] [PubMed]
     [Google Scholar]
  20. Thompson JD, Higgins DG, Gibson TJ. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 1994; 22:4673–4680 [View Article] [PubMed]
     [Google Scholar]
  21. Tamura K, Stecher G, Kumar S. MEGA11: Molecular Evolutionary Genetics Analysis version 11. Mol Biol Evol 2021; 38:3022–3027 [View Article] [PubMed]
     [Google Scholar]
  22. Saitou N, Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 1987; 4:406–425 [View Article] [PubMed]
     [Google Scholar]
  23. Felsenstein J. Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol 1981; 17:368–376 [View Article] [PubMed]
     [Google Scholar]
  24. Fitch WM. Toward defining the course of evolution: minimum change for a specific tree topology. Syst Biol 1971; 20:406–416 [View Article]
     [Google Scholar]
  25. Kimura M. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 1980; 16:111–120 [View Article] [PubMed]
     [Google Scholar]
  26. Felsenstein J. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 1985; 39:783–791 [View Article] [PubMed]
     [Google Scholar]
  27. Kim M, Oh HS, Park SC, Chun J. Towards a taxonomic coherence between average nucleotide identity and 16S rRNA gene sequence similarity for species demarcation of prokaryotes. Int J Syst Evol Microbiol 2014; 64:346–351 [View Article] [PubMed]
     [Google Scholar]
  28. Narsing Rao MP, Dong Z-Y, Kan Y, Dong L, Li S et al. Description of Paenibacillus tepidiphilus sp. nov., isolated from a tepid spring. Int J Syst Evol Microbiol 2020; 70:1977–1981 [View Article] [PubMed]
     [Google Scholar]
  29. Kovacs N. Identification of Pseudomonas pyocyanea by the oxidase reaction. Nature 1956; 178:703 [View Article] [PubMed]
     [Google Scholar]
  30. Thomas SH, Sanford RA, Amos BK, Leigh MB, Cardenas E et al. Unique ecophysiology among U(VI)-reducing bacteria as revealed by evaluation of oxygen metabolism in Anaeromyxobacter dehalogenans strain 2CP-C. Appl Environ Microbiol 2010; 76:176–183 [View Article] [PubMed]
     [Google Scholar]
  31. Collins MD, Pirouz T, Goodfellow M, Minnikin DE. Distribution of menaquinones in actinomycetes and corynebacteria. J Gen Microbiol 1977; 100:221–230 [View Article] [PubMed]
     [Google Scholar]
  32. Kroppenstedt RM. Separation of bacterial menaquinones by HPLC using reverse phase (RP18) and a silver loaded ion exchanger as stationary phases. J Liq Chromatogr 1982; 5:2359–2367 [View Article]
     [Google Scholar]
  33. Sasser M. Identification of bacteria by gas chromatography of cellular fatty acids. USFCC News 1990; 20:16
     [Google Scholar]
  34. Lovley DR, Giovannoni SJ, White DC, Champine JE, Phillips EJ et al. Geobacter metallireducens gen. nov. sp. nov., a microorganism capable of coupling the complete oxidation of organic compounds to the reduction of iron and other metals. Arch Microbiol 1993; 159:336–344 [View Article] [PubMed]
     [Google Scholar]
  35. Postgate JR. Chapter XIII the acetylene reduction test for nitrogen fixation. Methods Microbiol 1972; 6:343–356
     [Google Scholar]
  36. Yang S, Liu G-H, Tang R, Han S, Xie C-J et al. Description of two nitrogen-fixing bacteria, Geomonas fuzhouensis sp. nov. and Geomonas agri sp. nov., isolated from paddy soils. Antonie van Leeuwenhoek 2022; 115:435–444 [View Article] [PubMed]
     [Google Scholar]
  37. Nakajima A, Aono T, Tsukada S, Siarot L, Ogawa T et al. Lon protease of Azorhizobium caulinodans ORS571 is required for suppression of reb gene expression. Appl Environ Microbiol 2012; 78:6251–6261 [View Article] [PubMed]
     [Google Scholar]
  38. Luo R, Liu B, Xie Y, Li Z, Huang W et al. SOAPdenovo2: an empirically improved memory-efficient short-read de novo assembler. Gigascience 2012; 1:18 [View Article] [PubMed]
     [Google Scholar]
  39. Parks DH, Imelfort M, Skennerton CT, Hugenholtz P, Tyson GW. CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes. Genome Res 2015; 25:1043–1055 [View Article] [PubMed]
     [Google Scholar]
  40. Besemer J, Lomsadze A, Borodovsky M. GeneMarkS: a self-training method for prediction of gene starts in microbial genomes. Implications for finding sequence motifs in regulatory regions. Nucleic Acids Res 2001; 29:2607–2618 [View Article] [PubMed]
     [Google Scholar]
  41. Lowe TM, Eddy SR. tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res 1997; 25:955–964 [View Article] [PubMed]
     [Google Scholar]
  42. Lagesen K, Hallin P, Rødland EA, Staerfeldt H-H, Rognes T et al. RNAmmer: consistent and rapid annotation of ribosomal RNA genes. Nucleic Acids Res 2007; 35:3100–3108 [View Article] [PubMed]
     [Google Scholar]
  43. Kanehisa M, Goto S. KEGG: Kyoto Encyclopedia of Genes and Genomes. Nucleic Acids Res 2000; 28:27–30 [View Article] [PubMed]
     [Google Scholar]
  44. Kanehisa M, Goto S, Kawashima S, Okuno Y, Hattori M. The KEGG resource for deciphering the genome. Nucleic Acids Res 2004; 32:D277–D280 [View Article] [PubMed]
     [Google Scholar]
  45. Parks DH, Chuvochina M, Waite DW, Rinke C, Skarshewski A et al. A standardized bacterial taxonomy based on genome phylogeny substantially revises the tree of life. Nat Biotechnol 2018; 36:996–1004 [View Article] [PubMed]
     [Google Scholar]
  46. Yoon SH, Ha SM, Lim J, Kwon S, Chun J. A large-scale evaluation of algorithms to calculate average nucleotide identity. Antonie van Leeuwenhoek 2017; 110:1281–1286 [View Article] [PubMed]
     [Google Scholar]
  47. Meier-Kolthoff JP, Auch AF, Klenk H-P, Göker M. Genome sequence-based species delimitation with confidence intervals and improved distance functions. BMC Bioinformatics 2013; 14:60 [View Article] [PubMed]
     [Google Scholar]
  48. Cai X, Huang L, Yang G, Yu Z, Wen J et al. Transcriptomic, proteomic, and bioelectrochemical characterization of an exoelectrogen Geobacter soli grown with different electron acceptors. Front Microbiol 2018; 9:1075 [View Article] [PubMed]
     [Google Scholar]
  49. Goris J, Konstantinidis KT, Klappenbach JA, Coenye T, Vandamme P et al. DNA–DNA hybridization values and their relationship to whole-genome sequence similarities. Int J Syst Evol Microbiol 2007; 57:81–91 [View Article] [PubMed]
     [Google Scholar]
  50. Richter M, Rosselló-Móra R. Shifting the genomic gold standard for the prokaryotic species definition. Proc Natl Acad Sci U S A 2009; 106:19126–19131 [View Article] [PubMed]
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/ijsem/10.1099/ijsem.0.006268
Loading
Three Fe(III)-reducing and nitrogen-fixing bacteria, Anaeromyxobacter terrae sp. nov., Anaeromyxobacter oryzisoli sp. nov. and Anaeromyxobacter soli sp. nov., isolated from paddy soil
Int J Syst Evol Microbiol 74, 006268 (2024); https://doi.org/10.1099/ijsem.0.006268
/content/journal/ijsem/10.1099/ijsem.0.006268
/content/journal/ijsem/10.1099/ijsem.0.006268
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF

Most cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error