Skip to content
1887

Abstract

Denitrification is a vital link in the global bio-nitrogen cycle. Here, we isolated a strain (M9-3-2) that is a novel benzo[a]pyrene (BaP)-tolerant, anaerobic and aerobic denitrifying bacterium from a continuous BaP-enrichment cultured mangrove sediment. comparative genomics and taxonomic analysis clearly revealed that strain M9-3-2 (=MCCC 1K03313=JCM 32045) represents a novel species of a novel genus named as gen. nov., sp. nov., belonging to family , order . In addition, the species is transferred into genus and named comb. nov. The predominant respiratory quinone of strain M9-3-2 was ubiquinone-8 and the major polar lipids were diphosphatidylglycerol, phosphatidylethanolamine, phosphatidylglycerol, three unidentified phospholipids and three unidentified aminophospholipids. In this study, the capacity of strain M9-3-2 to eliminate nitrate was detected under anaerobic and aerobic conditions, and the removal rates of nitrate were 6.1×10 µg N/l/h/cell and 3×10 µg N/l/h/cell, respectively. Our results suggested that strain M9-3-2 could play an important role in the nitrogen removal regardless of the presence of oxygen in natural or/and man-made ecosystems.

Funding
This study was supported by the:
  • National Natural Science Foundation of China (Award 41976141)
    • Principle Award Recipient: YunTian
Loading

Article metrics loading...

/content/journal/ijsem/10.1099/ijsem.0.004946
2021-08-09
2025-05-17
Loading full text...

Full text loading...

/deliver/fulltext/ijsem/71/8/ijsem004946.html?itemId=/content/journal/ijsem/10.1099/ijsem.0.004946&mimeType=html&fmt=ahah

References

  1. Boden R. Reclassification of Thiobacillus aquaesulis (Wood & Kelly, 1995) as Annwoodia aquaesulis gen. nov., comb. nov., transfer of Thiobacillus (Beijerinck, 1904) from the Hydrogenophilales to the Nitrosomonadales, proposal of Hydrogenophilalia class. nov. within the ‘Proteobacteria’, and four new families within the orders Nitrosomonadales and Rhodocyclales; 2017; 671191–1205
  2. Rabus R, Wöhlbrand L, Thies D, Meyer M, Reinhold-Hurek B et al. Aromatoleum gen. nov., a novel genus accommodating the phylogenetic lineage including Azoarcus evansii and related species, and proposal of Aromatoleum aromaticum sp. nov., Aromatoleum petrolei sp. nov., Aromatoleum bremense sp. nov., Aromatoleum toluolicum sp. nov. and Aromatoleum diolicum sp. nov. Int J Syst Evol Microbiol 2019; 69:982–997 [View Article] [PubMed]
    [Google Scholar]
  3. Reinhold-Hurek B, Hurek T, Gillis M, Hoste B, Vancanneyt M et al. Azoarcus gen. nov., Nitrogen-fixing Proteobacteria associated with roots of kallar grass (Leptochloa fusca (L.) Kunth), and description of two species, Azoarcus indigens sp. nov and Azoarcus communis sp. nov.. Int J Syst Evol Microbiol 1993; 43:574–584
    [Google Scholar]
  4. Macy JM, Rech S, Auling G, Dorsch M, Stackebrandt E et al. Thauera selenatis gen. nov., sp. nov., a Member of the Beta Subclass of Proteobacteria with a novel type of anaerobic respiration. Int J Syst Evol Microbiol 1993; 43:135–142
    [Google Scholar]
  5. Weon HY, Kim BY, Yoo SH, Kwon SW, Go S-J et al. Uliginosibacterium gangwonense gen. nov., sp. nov., isolated from a wetland, Yongneup, in Korea. Int J Syst Evol Microbiol 2008; 58:131–135 [View Article] [PubMed]
    [Google Scholar]
  6. Itzigsohn H. Entwicklungsvorgange von Zoogloea, Oscillaria, Synedra, Staurastrum, Spirotaenia und Chroolepus [Development processes of Zoogloea, Oscillaria,Synedra, Staurastrum, Spirotaenia and Chroolepus]. In Sitzungs-Berichte Der Gesell-Schaft Naturforschender Freunde Zu [Meeting reports from the Society of Naturalists Friends] Berlin: 1868 pp 30–31
    [Google Scholar]
  7. Liu B, Mao Y, Bergaust L, Bakken LR, Frostegard A. Strains in the genus Thauera exhibit remarkably different denitrification regulatory phenotypes. Environ Microbiol 2013; 15:2816–2828 [View Article] [PubMed]
    [Google Scholar]
  8. Francis CA, Beman JM, Kuypers MMM. New processes and players in the nitrogen cycle: the microbial ecology of anaerobic and archaeal ammonia oxidation. ISME J 2007; 1:19–27 [View Article] [PubMed]
    [Google Scholar]
  9. Wang Z, Li W, Li H, Zheng W, Guo F. Phylogenomics of Rhodocyclales and its distribution in wastewater treatment systems. Sci Rep 2020; 10:3883 [View Article] [PubMed]
    [Google Scholar]
  10. Zhang T, Shao MF, Ye L. 454 Pyrosequencing reveals bacterial diversity of activated sludge from 14 sewage treatment plants. ISME J 2012; 6:1137–1147 [View Article] [PubMed]
    [Google Scholar]
  11. Jiang X, Ma M, Li J, Lu A, Zhong Z. Bacterial diversity of active sludge in wastewater treatment plant. Earth Sci Front 2008; 15:163–168
    [Google Scholar]
  12. Lu L, Wang B, Zhang Y, Xia L, An D et al. identification and nitrogen removal characteristics of Thauera sp. FDN-01 and application in sequencing batch biofilm reactor. SciTotal Environ 2019; 690:61–69
    [Google Scholar]
  13. Lee DJ, Wong BT, Adav SS. Azoarcus taiwanensis sp. nov., a denitrifying species isolated from a hot spring. Appl Microbiol Biotech 2014; 98:1301–1307
    [Google Scholar]
  14. Liao H, Li Y, Guo X, Lin X, Lai Q. Mangrovitalea sediminis gen. nov., sp. nov., a member of the family Alteromonadaceae isolated from mangrove sediment. Int J Syst Evol Microbiol 2017; 67:5172–5178
    [Google Scholar]
  15. Liao H, Li Y, Zhang M, Lin X, Lai Q et al. Altererythrobacter mangrovi sp. nov., isolated from mangrove sediment. Int J Syst Evol Microbiol 2017; 67:4851–4856 [View Article] [PubMed]
    [Google Scholar]
  16. Sasser M. Identification of Bacteria by Gas Chromatography of Cellular Fatty Acids, MIDI Technical Note 101. Newark, DE: MIDI Inc;
    [Google Scholar]
  17. Kates M. Techniques of Lipidology, 2nd. edn Amsterdam: Elsevier; 1985
    [Google Scholar]
  18. Collins M, Goodfellow M, Minnikin D. Isoprenoid quinone analysis in bacterial classification and identification. In Chemical Methods in Bacterial Systematics 1985 pp 267–287
    [Google Scholar]
  19. Li R, Zhu H, Ruan J, Qian W, Fang X et al. De novo assembly of human genomes with massively parallel short read sequencing. Genome Res 2010; 20:265–272 [View Article] [PubMed]
    [Google Scholar]
  20. Li R, Li Y, Kristiansen K, Wang J. SOAP: short oligonucleotide alignment program. Bioinformatics 2008; 24:713–714 [View Article] [PubMed]
    [Google Scholar]
  21. 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. Nucl Acid Res 2001; 29:2607–2618 [View Article]
    [Google Scholar]
  22. Kanehisa M, Goto S, Kawashima S, Okuno Y, Hattori M. The KEGG resource for deciphering the genome. Nucl Acid Res 2004; 32:D277
    [Google Scholar]
  23. Kanehisa M, Goto S, Hattori M, Aoki-Kinoshita KF, Itoh M et al. From genomics to chemical genomics: new developments in KEGG. Nucl Acid Res 2014; 34:D354
    [Google Scholar]
  24. Seemann T. Prokka: rapid prokaryotic genome annotation. Bioinformatics 2014; 30:2068–2069 [View Article] [PubMed]
    [Google Scholar]
  25. Yoon SH, Ha S-M, Kwon S, Lim J, Kim Y et al. Introducing EzBioCloud: A taxonomically united database of 16S rRNA and whole genome assemblies. Int J Syst Evol Microbiol 2017; 67:1613–1617 [View Article]
    [Google Scholar]
  26. Kumar S, Stecher G, Tamura K. MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for bigger datasets. Mol Biol Evol 2016; 33:1870–1874 [View Article] [PubMed]
    [Google Scholar]
  27. 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]
  28. 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]
  29. Tamura K, Nei M. Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol 1993; 10:512–526 [View Article] [PubMed]
    [Google Scholar]
  30. Felsenstein J. Confidence limits on phylogenies: An approach using the bootstrap. Evolution 1985; 39:783–791 [View Article]
    [Google Scholar]
  31. Page AJ, Cummins CA, Hunt M, Wong VK, Reuter S et al. Roary: rapid large-scale prokaryote pan genome analysis. Bioinformatics 2015; 31:3691–3693 [View Article] [PubMed]
    [Google Scholar]
  32. Liao H, Lin X, Li Y, Qu M, Tian Y. Reclassification of the Taxonomic framework of orders Cellvibrionales, Oceanospirillales, Pseudomonadales, and Alteromonadales in class Gammaproteobacteria through Phylogenomic Tree Analysis. mSystems 2020; 5:e00543–00520 [View Article] [PubMed]
    [Google Scholar]
  33. Stamatakis A. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 2006; 22:2688–2690 [View Article] [PubMed]
    [Google Scholar]
  34. Sullivan MJ, Petty NK, Beatson SA. Easyfig: a genome comparison visualizer. Bioinformatics 2006; 27:1009–1010 [View Article] [PubMed]
    [Google Scholar]
  35. Jain C, Rodriguez-R LM, Phillippy AM, Konstantinidis KT, Aluru S. High throughput ANI analysis of 90K prokaryotic genomes reveals clear species boundaries. Nat Comm 2018; 9:5114
    [Google Scholar]
  36. Dafner EV. Segmented continuous-flow analyses of nutrient in seawater: intralaboratory comparison of Technicon AutoAnalyzer II and Bran+Luebbe Continuous Flow AutoAnalyzer III. Limnology and Oceanography: Methods 2015; 13:511–520
    [Google Scholar]
  37. Ludwig W, Strunk O, Klugbauer N, Klugbauer N, Weizenegger M et al. Bacterial phylogeny based on comparative sequence analysis. Electrophoresis 1998; 19:554–568 [View Article] [PubMed]
    [Google Scholar]
  38. Chen D, Wang Z, Zhang M, Wang X, Lu S. IBV Strain C/N ratio on the performance and microbial community of a sequencing batch reactor. Environ Technol 20191–12
    [Google Scholar]
  39. Fu G, Yu X, Yu X-D, Zhao Z, Chen C et al. Azoarcus pumilus sp. nov., isolated from seawater in Sanya, China. Int J Syst Evol Microbiol 2019; 69:1459–1464 [View Article] [PubMed]
    [Google Scholar]
  40. 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]
  41. Li Y, Wang Y, Fu L, Gao Y, Zhao H et al. Aerobic-heterotrophic nitrogen removal through nitrate reduction and ammonium assimilation by marine bacterium Vibrio sp. Y1-5. Bioreso Technol 2017; 230:103–111
    [Google Scholar]
  42. Giannopoulos G, Sullivan MJ, Hartop KR, Rowley G, Gates AJ et al. Tuning the modular Paracoccus denitrificans respirome to adapt from aerobic respiration to anaerobic denitrification. Environ Microbiol 2017; 19:4953–4964 [View Article] [PubMed]
    [Google Scholar]
  43. Suenaga T, Hori T, Riya S, Hosomi M, Smets BF et al. Enrichment, isolation, and characterization of high-affinity N2O-reducing bacteria in a gas-permeable membrane reactor. Environ Sci Technol 2019; 53:12101–12112 [View Article]
    [Google Scholar]
  44. Zhang D, Han X, Zhou S, Yuan S, Peng S. Nitric oxide-dependent biodegradation of phenanthrene and fluoranthene: The co-occurrence of anaerobic and intra-aerobic pathways. Sc Total Environ 2021; 760:144032
    [Google Scholar]
  45. Martínez-Santos M, Lanzén A, Unda-Calvo J, Martín I, Garbisu C et al. Treated and untreated wastewater effluents alter river sediment bacterial communities involved in nitrogen and sulphur cycling. Sci Total Environ 2018; 633:1051–1061 [View Article]
    [Google Scholar]
  46. Wood DE, Lu J, Langmead B. Improved metagenomic analysis with Kraken 2. Genome Biol 2019; 20:257 [View Article] [PubMed]
    [Google Scholar]
  47. Beghini F, McIver LJ, Blanco-Míguez A, Dubois L, Asnicar F et al. Integrating taxonomic, functional, and strain-level profiling of diverse microbial communities with bioBakery 3. elife 2020; 10:e65088
    [Google Scholar]
  48. Yang L, Muhadesi JB, Wang MM, Wang B-J, Liu SJ et al. Thauera hydrothermalis sp. nov., a thermophilic bacterium isolated from hot spring. Int J Syst Evol Microbiol 2018; 68:3163–3168 [View Article] [PubMed]
    [Google Scholar]
/content/journal/ijsem/10.1099/ijsem.0.004946
Loading
/content/journal/ijsem/10.1099/ijsem.0.004946
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF

Supplementary material 2

EXCEL
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