1887

Abstract

A microaerophilic, Gram-negative, motile, and spiral-shaped bacterium, designated Y-M2, was isolated from oil sludge of Shengli oil field. The optimal growth condition of strain Y-M2 was at 25 °C, pH 7.0, and in the absence of NaCl. The major polar lipid was phosphatidylethanolamine. The main cellular fatty acid was iso-C 3-OH. It contained Q-9 and Q-10 as the predominant quinones. The DNA G+C content was 68.1 mol%. Strain Y-M2 showed the highest 16S rRNA gene sequence similarity to 26-4b (91.1 %). Phylogenetic analyses based on 16S rRNA gene and genomes showed that strain Y-M2 formed a distinct cluster in the order . Genomic analysis showed that Y-M2 possesses a complete nitrogen-fixation cluster which is phylogenetically close to that of methanogene. The cluster, encompassing the nitrogenase genes, was found in every N-fixing strain within the order . Phylogeny, phenotype, chemotaxonomy, and genomic results demonstrated that strain Y-M2 represents a novel species of a novel genus in a novel family fam. nov. in the order , for which the name gen. nov., sp. nov. was proposed. The type strain is Y-M2 (=CCAM 827=JCM 34765).

Funding
This study was supported by the:
  • National Nature Science Foundation of China (Award 92051108)
    • Principle Award Recipient: LeiCheng
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License. This article was made open access via a Publish and Read agreement between the Microbiology Society and the corresponding author’s institution.
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2024-03-21
2024-06-18
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References

  1. Cordeiro AB, Ribeiro RA, Helene LCF, Hungria M. Rhizobium esperanzae sp. nov., a N2-fixing root symbiont of Phaseolus vulgaris from Mexican soils. Int J Syst Evol Microbiol 2017; 67:3937–3945 [View Article] [PubMed]
    [Google Scholar]
  2. Divyasree B, Lakshmi K, Bharti D, Sasikala C, Ramana CV. Caenispirillum deserti sp. nov., a spheroplast-forming bacterium isolated from a salt desert. Int J Syst Evol Microbiol 2015; 65:3119–3124 [View Article] [PubMed]
    [Google Scholar]
  3. Yoo S-H, Weon H-Y, Noh H-J, Hong S-B, Lee C-M et al. Roseomonas aerilata sp. nov., isolated from an air sample. Int J Syst Evol Microbiol 2008; 58:1482–1485 [View Article] [PubMed]
    [Google Scholar]
  4. Yang Y, Zhang R, Feng J, Wang C, Chen J. Azospirillum griseum sp. nov., isolated from lakewater. Int J Syst Evol Microbiol 2019; 69:3676–3681 [View Article] [PubMed]
    [Google Scholar]
  5. Baik KS, Hwang YM, Choi J-S, Kwon J, Seong CN. Dongia rigui sp. nov., isolated from freshwater of a large wetland in Korea. Antonie van Leeuwenhoek 2013; 104:1143–1150 [View Article] [PubMed]
    [Google Scholar]
  6. Zhou S, Han L, Wang Y, Yang G, Zhuang L et al. Azospirillum humicireducens sp. nov., a nitrogen-fixing bacterium isolated from a microbial fuel cell. Int J Syst Evol Microbiol 2013; 63:2618–2624 [View Article] [PubMed]
    [Google Scholar]
  7. Young CC, Hupfer H, Siering C, Ho M-J, Arun AB et al. Azospirillum rugosum sp. nov., isolated from oil-contaminated soil. Int J Syst Evol Microbiol 2008; 58:959–963 [View Article] [PubMed]
    [Google Scholar]
  8. Wu D, Zhang X-J, Liu H-C, Zhou Y-G, Wu X-L et al. Azospirillum oleiclasticum sp. nov, a nitrogen-fixing and heavy oil degrading bacterium isolated from an oil production mixture of Yumen oilfield. Syst Appl Microbiol 2021; 44:126171 [View Article] [PubMed]
    [Google Scholar]
  9. Coenye T, Goris J, Spilker T, Vandamme P, LiPuma JJ. Characterization of unusual bacteria isolated from respiratory secretions of cystic fibrosis patients and description of Inquilinus limosus gen. nov., sp. nov. J Clin Microbiol 2002; 40:2062–2069 [View Article] [PubMed]
    [Google Scholar]
  10. Yoon JH, Kang SJ, Park S, Oh TK. Caenispirillum bisanense gen. nov., sp. nov., isolated from sludge of a dye works. Int J Syst Evol Microbiol 2007; 57:1217–1221 [View Article] [PubMed]
    [Google Scholar]
  11. Dziuba M, Koziaeva V, Grouzdev D, Burganskaya E, Baslerov R et al. Magnetospirillum caucaseum sp. nov., Magnetospirillum marisnigri sp. nov. Int J Syst Evol Microbiol 2016; 66:2069–2077 [View Article]
    [Google Scholar]
  12. Humrighouse BW, Emery BD, Kelly AJ, Metcalfe MG, Mbizo J et al. Haematospirillum jordaniae gen. nov., sp. nov., isolated from human blood samples. Antonie van Leeuwenhoek 2016; 109:493–500
    [Google Scholar]
  13. Tikhonova EN, Grouzdev DS, Kravchenko IK. Azospirillum palustre sp. nov., a methylotrophic nitrogen-fixing species isolated from raised bog. Int J Syst Evol Microbiol 2019; 69:2787–2793 [View Article] [PubMed]
    [Google Scholar]
  14. Hördt A, López MG, Meier-Kolthoff JP, Schleuning M, Weinhold L-M et al. Analysis of 1,000+ type-strain genomes substantially improves taxonomic classification of Alphaproteobacteria. Front Microbiol 2020; 11:468 [View Article] [PubMed]
    [Google Scholar]
  15. Koziaeva VV, Sorokin DY, Kolganova TV, Grouzdev DS. Magnetospirillum sulfuroxidans sp. nov., capable of sulfur-dependent lithoautotrophy and a taxonomic reevaluation of the order Rhodospirillales. Syst Appl Microbiol 2023; 46:126406 [View Article] [PubMed]
    [Google Scholar]
  16. Urdiain M, López-López A, Gonzalo C, Busse H-J, Langer S et al. Reclassification of Rhodobium marinum and Rhodobium pfennigii as Afifella marina gen. nov. comb. nov. and Afifella pfennigii comb. nov., a new genus of photoheterotrophic Alphaproteobacteria and emended descriptions of Rhodobium, Rhodobium orientis and Rhodobium gokarnense. Syst Appl Microbiol 2008; 31:339–351 [View Article] [PubMed]
    [Google Scholar]
  17. Guyoneaud R, Mouné S, Eatock C, Bothorel V, Hirschler-Réa A et al. Characterization of three spiral-shaped purple nonsulfur bacteria isolated from coastal lagoon sediments, saline sulfur springs, and microbial mats: emended description of the genus Roseospira and description of Roseospira marina sp. nov., Roseospira navarrensis sp. nov., and Roseospira thiosulfatophila sp. nov. Arch Microbiol 2002; 178:315–324 [View Article] [PubMed]
    [Google Scholar]
  18. Kalyan Chakravarthy S, Srinivas TNR, Anil Kumar P, Sasikala C, Ramana CV. Roseospira visakhapatnamensis sp. nov. and Roseospira goensis sp. nov. Int J Syst Evol Microbiol 2007; 57:2453–2457 [View Article] [PubMed]
    [Google Scholar]
  19. Xie CH, Yokota A. Azospirillum oryzae sp. nov., a nitrogen-fixing bacterium isolated from the roots of the rice plant Oryza sativa. Int J Syst Evol Microbiol 2005; 55:1435–1438 [View Article] [PubMed]
    [Google Scholar]
  20. Eckert B, Weber OB, Kirchhof G, Halbritter A, Stoffels M et al. Azospirillum doebereinerae sp. nov., a nitrogen-fixing bacterium associated with the C4-grass Miscanthus. Int J Syst Evol Microbiol 2001; 51:17–26 [View Article] [PubMed]
    [Google Scholar]
  21. Tarrand JJ, Krieg NR, Döbereiner J. A taxonomic study of the Spirillum lipoferum group, with descriptions of a new genus, Azospirillum gen. nov. and two species, Azospirillum lipoferum (Beijerinck) comb. nov. and Azospirillum brasilense sp. nov. Can J Microbiol 1978; 24:967–980 [View Article] [PubMed]
    [Google Scholar]
  22. Parsons C, Stüeken EE, Rosen CJ, Mateos K, Anderson RE. Radiation of nitrogen-metabolizing enzymes across the tree of life tracks environmental transitions in Earth history. Geobiology 2021; 19:18–34 [View Article] [PubMed]
    [Google Scholar]
  23. Jasniewski AJ, Lee CC, Ribbe MW, Hu Y. Reactivity, mechanism, and assembly of the alternative nitrogenases. Chem Rev 2020; 120:5107–5157 [View Article] [PubMed]
    [Google Scholar]
  24. Affourtit J, Zehr JP, Paerl HW. Distribution of nitrogen-fixing microorganisms along the Neuse River Estuary, North Carolina. Microb Ecol 2001; 41:114–123 [View Article] [PubMed]
    [Google Scholar]
  25. Dong X, Zhang C, Peng Y, Zhang H-X, Shi L-D et al. Phylogenetically and catabolically diverse diazotrophs reside in deep-sea cold seep sediments. Nat Commun 2022; 13:4885 [View Article] [PubMed]
    [Google Scholar]
  26. Mahmud K, Makaju S, Ibrahim R, Missaoui A. Current progress in nitrogen fixing plants and microbiome research. Plants 2020; 9:97 [View Article] [PubMed]
    [Google Scholar]
  27. Zhang X, Hu W, Jin X, Chen T, Niu Y. Diversity of soil nitrogen-fixing bacteria in the rhizosphere and non-rhizophere soils of Ebinur Lake Wetland. Arch Microbiol 2021; 203:3919–3932 [View Article] [PubMed]
    [Google Scholar]
  28. Sizova MV, Panikov NS, Spiridonova EM, Slobodova NV, Tourova TP. Novel facultative anaerobic acidotolerant Telmatospirillum siberiense gen. Syst Appl Microbiol 2007; 30:213–220
    [Google Scholar]
  29. Yan Y, Yang J, Dou Y, Chen M, Ping S et al. Nitrogen fixation island and rhizosphere competence traits in the genome of root-associated Pseudomonas stutzeri A1501. Proc Natl Acad Sci U S A 2008; 105:7564–7569 [View Article] [PubMed]
    [Google Scholar]
  30. Lalucat J, Gomila M, Mulet M, Zaruma A, García-Valdés E. Past, present and future of the boundaries of the Pseudomonas genus: proposal of Stutzerimonas gen. nov. Syst Appl Microbiol 2022; 45:126289 [View Article] [PubMed]
    [Google Scholar]
  31. Li F-L, Wang X-T, Shan J-J, Li S, Zhang Y-X et al. Oleiliquidispirillum nitrogeniifigens gen. nov., sp. nov., a new member of the family Rhodospirillaceae isolated from oil reservoir water. Int J Syst Evol Microbiol 2020; 70:3468–3474 [View Article] [PubMed]
    [Google Scholar]
  32. Zhang X, Tu B, Dai L-R, Lawson PA, Zheng Z-Z et al. Petroclostridium xylanilyticum gen. nov., sp. nov., a xylan-degrading bacterium isolated from an oilfield, and reclassification of clostridial cluster III members into four novel genera in a new Hungateiclostridiaceae fam. nov. Int J Syst Evol Microbiol 2018; 68:3197–3211 [View Article] [PubMed]
    [Google Scholar]
  33. Weisburg WG, Barns SM, Pelletier DA, Lane DJ. 16S ribosomal DNA amplification for phylogenetic study. J Bacteriol 1991; 173:697–703 [View Article] [PubMed]
    [Google Scholar]
  34. Edgar RC. MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics 2004; 5:1–19 [View Article] [PubMed]
    [Google Scholar]
  35. Price MN, Dehal PS, Arkin AP. FastTree 2--approximately maximum-likelihood trees for large alignments. PLoS One 2010; 5:e9490 [View Article] [PubMed]
    [Google Scholar]
  36. Nguyen L-T, Schmidt HA, von Haeseler A, Minh BQ. IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol Biol Evol 2015; 32:268–274 [View Article] [PubMed]
    [Google Scholar]
  37. Yarza P, Yilmaz P, Pruesse E, Glöckner FO, Ludwig W et al. Uniting the classification of cultured and uncultured bacteria and archaea using 16S rRNA gene sequences. Nat Rev Microbiol 2014; 12:635–645 [View Article] [PubMed]
    [Google Scholar]
  38. Yoon S-H, Ha S-M, 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]
  39. Yang M, Li J, Lv X, Dai L, Wu K et al. Thermosynergistes pyruvativorans gen. nov., sp. nov., an anaerobic, pyruvate-degrading bacterium from Shengli oilfield, and proposal of Thermosynergistaceae fam. nov. in the phylum Synergistetes. Int J Syst Evol Microbiol 2021; 71: [View Article]
    [Google Scholar]
  40. Hyatt D, Chen G-L, Locascio PF, Land ML, Larimer FW et al. Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC Bioinformatics 2010; 11:119 [View Article] [PubMed]
    [Google Scholar]
  41. Aramaki T, Blanc-Mathieu R, Endo H, Ohkubo K, Kanehisa M et al. KofamKOALA: KEGG ortholog assignment based on profile HMM and adaptive score threshold. Bioinformatics 2020; 36:2251–2252 [View Article] [PubMed]
    [Google Scholar]
  42. Garcia AK, McShea H, Kolaczkowski B, Kaçar B. Reconstructing the evolutionary history of nitrogenases: evidence for ancestral molybdenum-cofactor utilization. Geobiology 2020; 18:394–411 [View Article] [PubMed]
    [Google Scholar]
  43. Normand P, Bousquet J. Phylogeny of nitrogenase sequences in Frankia and other nitrogen-fixing microorganisms. J Mol Evol 1989; 29:436–447 [View Article] [PubMed]
    [Google Scholar]
  44. Normand P, Gouy M, Cournoyer B, Simonet P. Nucleotide sequence of nifD from Frankia alni strain ArI3: phylogenetic inferences. Mol Biol Evol 1992; 9:495–506 [View Article] [PubMed]
    [Google Scholar]
  45. Hartmann LS, Barnum SR. Inferring the evolutionary history of Mo-dependent nitrogen fixation from phylogenetic studies of nifK and nifDK. J Mol Evol 2010; 71:70–85 [View Article] [PubMed]
    [Google Scholar]
  46. Pence N, Lewis N, Alleman AB, Seefeldt LC, Peters JW. Revealing a role for the G subunit in mediating interactions between the nitrogenase component proteins. J Inorg Biochem 2021; 214:111273 [View Article] [PubMed]
    [Google Scholar]
  47. Boyd ES, Hamilton TL, Peters JW. An alternative path for the evolution of biological nitrogen fixation. Front Microbiol 2011; 2:205 [View Article] [PubMed]
    [Google Scholar]
  48. Fan H, Li J, Wu W, Chen R, Yang M et al. Description of a moderately acidotolerant and aerotolerant anaerobic bacterium Acidilutibacter cellobiosedens gen. nov., sp. nov. within the family Acidilutibacteraceae fam. nov., and proposal of Sporanaerobacteraceae fam. nov. and Tepidimicrobiaceae fam. nov. Syst Appl Microbiol 2023; 46:126376 [View Article] [PubMed]
    [Google Scholar]
  49. Sasser M. Identification of bacteria by gas chromatography of cellular fatty acids. USFCC Newsl 1990; 20:1–6
    [Google Scholar]
  50. Komagata K SK. 4 Lipid and cell-wall analysis in bacterial systematics. In Colwell RR, Grigorova R (eds) Methods in Microbiology Academic Press; 1988 pp 161–207
    [Google Scholar]
  51. Tindall BJ. A comparative study of the lipid composition of Halobacterium saccharovorum from various sources. Syst and Appl Microbiol 1990; 13:128–130 [View Article]
    [Google Scholar]
  52. Kates M. Techniques of Lipidology, 2nd edn Amsterdam: Elsevier; 1986 pp 106–107
    [Google Scholar]
  53. Garrity G. Alphaproteobacteria class. nov. In Brenner DJ, Krieg NR, Staley JT. eds Bergey’s Manual of Systematic Bacteriology: Volume TwoThe Proteobacteria Part C The Alpha-, Beta-, Delta-, and Epsilonproteobacteria Boston, MA: Springer US; 2005 pp 1–574
    [Google Scholar]
  54. Foesel BU, Gössner AS, Drake HL, Schramm A. Geminicoccus roseus gen. nov., sp. nov., an aerobic phototrophic Alphaproteobacterium isolated from a marine aquaculture biofilter. Syst Appl Microbiol 2007; 30:581–586 [View Article] [PubMed]
    [Google Scholar]
  55. Wiese J, Thiel V, Gärtner A, Schmaljohann R, Imhoff JF. Kiloniella laminariae gen. nov., sp. nov., an Alphaproteobacterium from the marine macroalga Laminaria saccharina. Int J Syst Evol Microbiol 2009; 59:350–356 [View Article] [PubMed]
    [Google Scholar]
  56. Yoon J, Kang D-H. Terasakiella salincola sp. nov., a marine Alphaproteobacterium isolated from seawater, and emended description of the genus Terasakiella. Int J Syst Evol Microbiol 2018; 68:2048–2053 [View Article] [PubMed]
    [Google Scholar]
  57. Zhang GI, Hwang CY, Cho BC. Thalassobaculum litoreum gen. nov., sp. nov., a member of the family Rhodospirillaceae isolated from coastal seawater. Int J Syst Evol Microbiol 2008; 58:479–485 [View Article] [PubMed]
    [Google Scholar]
  58. López-López A, Pujalte MJ, Benlloch S, Mata-Roig M, Rosselló-Mora R et al. Thalassospira lucentensis gen. nov., sp. nov., a new marine member of the alpha-proteobacteria. Int J Syst Evol Microbiol 2002; 52:1277–1283 [View Article] [PubMed]
    [Google Scholar]
  59. Thrash JC, Ahmadi S, Torok T, Coates JD. Magnetospirillum bellicus sp. nov., a novel dissimilatory perchlorate-reducing Alphaproteobacterium isolated from a bioelectrical reactor. Appl Environ Microbiol 2010; 76:4730–4737 [View Article] [PubMed]
    [Google Scholar]
  60. Imhoff JF, Petri R, Suling J. Reclassification of species of the spiral-shaped phototrophic purple non-sulfur bacteria of the alpha-proteobacteria: description of the new genera Phaeospirillum gen. Int J Syst Bacteriol 1998; 48:793–798 [View Article] [PubMed]
    [Google Scholar]
  61. Humrighouse BW, Emery BD, Kelly AJ, Metcalfe MG, Mbizo J et al. Erratum to: Haematospirillum jordaniae gen. nov., sp. nov., isolated from human blood samples. Antonie van Leeuwenhoek 2016; 109:895–896 [View Article] [PubMed]
    [Google Scholar]
  62. Lai Q, Yuan J, Gu L, Shao Z. Marispirillum indicum gen. nov., sp. nov., isolated from a deep-sea environment. Int J Syst Evol Microbiol 2009; 59:1278–1281 [View Article] [PubMed]
    [Google Scholar]
  63. Yoon JH, Kang SJ, Park S, Lee SY, Oh TK. Reclassification of Aquaspirillum itersonii and Aquaspirillum peregrinum as Novispirillum itersonii gen. nov., comb. nov. and Insolitispirillum peregrinum gen. nov., comb. nov. Int J Syst Evol Microbiol 2007; 57:2830–2835 [View Article] [PubMed]
    [Google Scholar]
  64. Tang K, Yang L-H, Chen Y-P, Tao Y, Feng F-Y et al. Aerophototrophica crusticola gen. nov., sp. nov., isolated from desert biocrusts. Int J Syst Evol Microbiol 2019; 71: [View Article] [PubMed]
    [Google Scholar]
  65. Wang Z, Zhang Z, Li C, Zhang M, Zhao D et al. Algihabitans albus gen. nov., sp. nov., isolated from a culture of the green alga Ulva prolifera. Int J Syst Evol Microbiol 2019; 69:828–832 [View Article] [PubMed]
    [Google Scholar]
  66. Wang G, Tang D, Li G, Xu S, Dang G et al. Denitrobaculum tricleocarpae gen. nov., sp. nov., a marine bacterium from coralline algae tricleocarpa sp. Int J Syst Evol Microbiol 2020; 70:3335–3339 [View Article] [PubMed]
    [Google Scholar]
  67. Wang S, Ye Z-H, Wang N-N, Mu D-S, Du Z-J. Ferruginivarius sediminum gen. nov., sp. nov., isolated from a marine solar saltern. Int J Syst Evol Microbiol 2019; 69:3056–3061 [View Article] [PubMed]
    [Google Scholar]
  68. Kim J, Jeong SE, Khan SA, Jeon CO. Hwanghaeella grinnelliae gen. nov., sp. nov., isolated from a marine red alga. Int J Syst Evol Microbiol 2019; 69:3544–3550 [View Article]
    [Google Scholar]
  69. Chen RW, Wang KX, Zhou XF, Long C, Tian XP et al. Indioceanicola profundi gen. nov., sp. nov., isolated from Indian Ocean sediment. Int J Syst Evol Microbiol 2018; 68:3707–3712
    [Google Scholar]
  70. Lakshmi KVNS, Divyasree B, Ramprasad EVV, Sasikala C, Ramana CV. Reclassification of Rhodospirillum photometricum Molisch 1907, Rhodospirillum sulfurexigens Anil Kumar et al. 2008 and Rhodospirillum oryzae Lakshmi et al. 2013 in a new genus, Pararhodospirillum gen. nov., as Pararhodospirillum photometricum comb. nov., Pararhodospirillum sulfurexigens comb. nov. and Pararhodospirillum oryzae comb. nov., respectively, and emended description of the genus Rhodospirillum. Int J Syst Evol Microbiol 2014; 64:1154–1159 [View Article] [PubMed]
    [Google Scholar]
  71. Lakshmi KVNS, Sasikala C, Ashok Kumar GV, Chandrasekaran R, Ramana CV. Phaeovibrio sulfidiphilus gen. nov., sp. nov., phototrophic alphaproteobacteria isolated from brackish water. Int J Syst Evol Microbiol 2011; 61:828–833 [View Article] [PubMed]
    [Google Scholar]
  72. Pfennig N, Lünsdorf H, Süling J, Imhoff JF. Rhodospira trueperi gen. nov., spec. nov., a new phototrophic Proteobacterium of the alpha group. Arch Microbiol 1997; 168:39–45 [View Article] [PubMed]
    [Google Scholar]
  73. Anil Kumar P, Aparna P, Srinivas TNR, Sasikala C, Ramana CV. Rhodospirillum sulfurexigens sp. nov., a phototrophic alphaproteobacterium requiring a reduced sulfur source for growth. Int J Syst Evol Microbiol 2008; 58:2917–2920 [View Article] [PubMed]
    [Google Scholar]
  74. Dar Jean W, Huang SP, Chen JS, Shieh WY. Tagaea marina gen. nov., sp. nov., a marine bacterium isolated from shallow coastal water. Int J Syst Evol Microbiol 2016; 66:592–597 [View Article] [PubMed]
    [Google Scholar]
  75. Lin SY, Hameed A, Tsai CF, Young CC. Vineibacter terrae gen. nov., sp. nov., an ammonium-assimilating and nitrate-reducing bacterium isolated from vineyard soil. Int J Syst Evol Microbiol 2021; 71:12 [View Article] [PubMed]
    [Google Scholar]
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