Abstract
A Gram-stain-negative, oxidase-negative, rod-shaped, motile, facultatively anaerobic bacterial strain, designated as CY1220T, was isolated from an anaerobic fermentation liquid of food waste treatment plant. Phylogenetic analysis based on 16S rRNA gene sequences indicated that the strain CY1220T belongs to the genus Thiopseudomonas, with the highest sequence similarity to Thiopseudomonas alkaliphila B4199T (95.91%), followed by Thiopseudomonas denitrificans X2T (95.56%). The genomic DNA G + C content of strain CY1220T was 48.6 mol%. The average nucleotide identity values and digital DNA–DNA hybridization values between strain CY1220T and the type species of T. alkaliphila and T. denitrificans were in the range of 70.8–71.6% and 19.2–20.0%, respectively, below the thresholds for species delineation. The strain was able to grow utilizing acetic acid and butyric acid (AABA) as the sole carbon source in aerobic conditions. Genomic analysis predicted that the strain could synthesize vitamin B12 and ectoine. The predominant cellular fatty acids were C18:1 ω7c and/or C18:1 ω6c, C16:0, C16:1 ω7c and/or C16:1 ω6c and C12:0. The polar lipids comprised diphosphatidylglycerol, unknown polar lipid, phosphatidylethanolamine, phosphatidylglycerol, and phospholipid. Q-8 (2.1%) and Q-9 (97.9%) were detected as the respiratory quinones. Based on its phenotypic, genotypic and genomic characteristics, strain CY1220T represents a novel species in the genus Thiopseudomonas, for which the name Thiopseudomonas acetoxidans sp. nov. is proposed. The type strain is CY1220T (= GDMCC 1.3503 T = JCM 35747 T).
Similar content being viewed by others
Data availability
The 16S rRNA gene sequence of Thiopseudomonas acetoxidans CY1220T has been assigned the accession number OQ842236 in the GenBank database of the NCBI. The draft genome sequences of CY1220T have been deposited under the accession number JAUCDY000000000.
References
Alanjary M, Steinke K, Ziemert N (2019) AutoMLST: an automated web server for generating multi-locus species trees highlighting natural product potential. Nucleic Acids Res 47:W276-w282. https://doi.org/10.1093/nar/gkz282
Antonov IV (2020) Two cobalt chelatase subunits can be generated from a single chlD gene via programed frameshifting. Mol Biol Evol 37:2268–2278. https://doi.org/10.1093/molbev/msaa081
Aziz RK, Bartels D, Best AA, DeJongh M, Disz T, EdwarRA FK, Gerdes S, Glass EM, Kubal M, Meyer F, Olsen GJ, Olson R, Osterman AL, Overbeek RA, McNeilLK PD, Paczian T, Parrello B, Pusch GD, ReichC SR, Vassieva O, Vonstein V, Wilke A, Zagnitko O (2008) The RAST Server: rapid annotations usingsubsystemstechnology. BMC Genomics 9:75. https://doi.org/10.1186/1471-2164-9-75
Becker D, Popp D, Bonk F, Kleinsteuber S, Harms H, Centler F (2023) Metagenomic analysis of anaerobic microbial communities degrading short-chain fatty acids as sole carbon sources. Microorganisms 11:420. https://doi.org/10.3390/microorganisms11020420
Bertelli C, Laird MR, Williams KP, Simon Fraser University ResearchComputing Group, Lau BY, Hoad G, Winsor GL, Brinkman FSL (2017) IslandViewer 4: expandedprediction of genomic islands for larger-scale datasets. Nucleic Acids Res 45:W30-35. https://doi.org/10.1093/nar/gkx343
Blin K, Shaw S, Augustijn HE, Reitz ZL, Biermann F, Alanjary M, Fetter A, Terlouw BR, Metcalf WW, Helfrich EJN, van Wezel GP, Medema MH, Weber T (2023) antiSMASH 7.0: new and improved predictions for detection, regulation, chemical structures and visualisation. Nucleic Acids Res 51:W46–W50. https://doi.org/10.1093/nar/gkad344
Chan PP, Lowe TM (2019) tRNAscan-SE: Searching for tRNA genes in genomic sequences. Methods Mol Biol 1962:1–14. https://doi.org/10.1007/978-1-4939-9173-0_1
Chaumeil PA, Mussig AJ, Hugenholtz P, Parks DH (2019) GTDB-Tk: a toolkit to classify genomes with the Genome Taxonomy Database. Bioinformatics 36:1925–1927. https://doi.org/10.1093/bioinformatics/btz848
Chen S, Zhou Y, Chen Y, Gu J (2018) fastp: an ultra-fast all-in-one FASTQ preprocessor. Bioinformatics 34:i884–i890. https://doi.org/10.1093/bioinformatics/bty560
Chun J, Oren A, Ventosa A, Christensen H, Arahal DR, da Costa MS, Rooney AP, Yi H, Xu XW, De Meyer S, 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. https://doi.org/10.1099/ijsem.0.002516
Drobish AM, Emery BD, Whitney AM, Lauer AC, Metcalfe MG, McQuiston JR (2016) Oblitimonas alkaliphila gen. nov., sp. nov., in the family Pseudomonadaceae, recovered from a historical collection of previously unidentified clinical strains. Int J Syst Evol Microbiol 66:3063–3070. https://doi.org/10.1099/ijsem.0.001147
Fatollahi P, Ghasemi M, Yazdian F, Sadeghi A (2021) Ectoine production in bioreactor by Halomonas elongata DSM2581: Using MWCNT and Fe-nanoparticle. Biotechnol Prog 37:e3073. https://doi.org/10.1002/btpr.3073
Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791. https://doi.org/10.1111/j.1558-5646.1985.tb00420.x
Fitch WM (1971) Toward defining the course of evolution: minimum change for a specific tree topology. Syst Biol 20:406–416. https://doi.org/10.2307/2412116
Gervasoni S, Malloci G, Bosin A, Vargiu AV, Zgurskaya HI, Ruggerone P (2022) Recognition of quinolone antibiotics by the multidrug efflux transporter MexB of Pseudomonas aeruginosa. Phys Chem Chem Phys 24:16566–16575. https://doi.org/10.1039/d2cp00951j
Grant JR, Stothard P (2008) The CGView Server: a comparative genomics tool for circular genomes. Nucleic Acids Res 36:W181-184. https://doi.org/10.1093/nar/gkn179
Huerta-Cepas J, Szklarczyk D, Heller D, Hernández-Plaza A, Forslund SK, Cook H, Mende DR, Letunic I, Rattei T, Jensen LJ, von Mering C, Bork P (2019) eggNOG 5.0: a hierarchical, functionally and phylogenetically annotated orthology resource based on 5090 organisms and 2502 viruses. Nucleic Acids Res 47:D309–D314. https://doi.org/10.1093/nar/gky1085
Jia B, Raphenya AR, Alcock B, Waglechner N, Guo P, TsangKK LBA, Dave BM, Pereira S, Sharma AN, DoshiS CM, Lo R, Williams LE, Frye JG, Elsayegh T, Sardar D, Westman EL, Pawlowski AC, Johnson TA, Brinkman FS, Wright GD, McArthur AG (2017) CARD2017: expansion and model-centric curation of the comprehensiveantibiotic resistance database. Nucleic AcidsRes 45:D566-573. https://doi.org/10.1093/nar/gkw1004
Jiang CY, Liu Y, Liu YY, You XY, Guo X, Liu SJ (2008) Alicyclobacillus ferrooxydans sp. nov., a ferrous-oxidizing bacterium from solfataric soil. Int J Syst Evol Microbiol 58:2898–2903. https://doi.org/10.1099/ijs.0.2008/000562-0
Kellogg JA, Bankert DA, Withers GS, Sweimler W, Kiehn TE, Pfyffer GE (2001) Application of the Sherlock Mycobacteria Identification System using high-performance liquid chromatography in a clinical laboratory. J Clin Microbiol 39:964–970. https://doi.org/10.1128/jcm.39.3.964-970.2001
Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120. https://doi.org/10.1007/BF01731581
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. https://doi.org/10.1093/molbev/msy096
Lagesen K, Hallin P, Rødland EA, Staerfeldt HH, Rognes T, Ussery DW (2007) RNAmmer: consistent and rapid annotation of ribosomal RNA genes. Nucleic Acids Res 35:3100–3108. https://doi.org/10.1093/nar/gkm160
Liu W, Cong B, Lin J, Zhao L, Liu S (2022) Complete genome sequencing and comparison of two nitrogen-metabolizing bacteria isolated from Antarctic deep-sea sediment. BMC Genomics 23:713. https://doi.org/10.1186/s12864-022-08942-6
Liu T, Ning L, Mei C, Li S, Zheng L, Qiao P, Wang H, Hu T, Zhong W (2023) Synthetic bacterial consortia enhanced the degradation of mixed priority phthalate ester pollutants. Environ Res 235:116666. https://doi.org/10.1016/j.envres.2023.116666
Luo R, Liu B, Xie Y, Li Z, Huang W, Yuan J, He G, Chen Y, Pan Q, Liu Y, Tang J, Wu G, Zhang H, Shi Y, Liu Y, Yu C, Wang B, Lu Y, Han C, Cheung DW, Yiu SM, Peng S, Xiaoqian Z, Liu G, Liao X, Li Y, Yang H, Wang J, Lam TW, Wang J (2012) SOAPdenovo2: an empirically improved memory-efficient short-read de novo assembler. Gigascience 1:18. https://doi.org/10.1186/2047-217x-1-18
Luo C, Rodriguez RL, Konstantinidis KT (2014) MyTaxa: an advanced taxonomic classifier for genomic and metagenomic sequences. Nucleic Acids Res 42:e73. https://doi.org/10.1093/nar/gku169
Meier-Kolthoff JP, Auch AF, Klenk HP, Göker M (2013) Genome sequence-based species delimitation with confidence intervals and improved distance functions. BMC Bioinformatics 14:60. https://doi.org/10.1186/1471-2105-14-60
Nagakubo S, Nishino K, Hirata T, Yamaguchi A (2002) The putative response regulator BaeR stimulates multidrug resistance of Escherichia coli via a novel multidrug exporter system, MdtABC. J Bacteriol 184:4161–4167. https://doi.org/10.1128/jb.184.15.4161-4167.2002
Orans J, Johnson MD, Coggan KA, Sperlazza JR, Heiniger RW, Wolfgang MC, Redinbo MR (2010) Crystal structure analysis reveals Pseudomonas PilY1 as an essential calcium-dependent regulator of bacterial surface motility. Proc Natl Acad Sci U S A 107:1065–1070. https://doi.org/10.1073/pnas.0911616107
Parks DH, Imelfort M, Skennerton CT, Hugenholtz P, Tyson GW (2015) CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes. Genome Res 25:1043–1055. https://doi.org/10.1101/gr.186072.114
Qin H, Wang D, Xing X, Tang Y, Wei X, Chen X, Zhang W, Chen A, Li L, Liu Y, Zhu B (2021) A few key nirK- and nosZ-denitrifier taxa play a dominant role in moisture-enhanced N2O emissions in acidic paddy soil. Geoderma 385:114917. https://doi.org/10.1016/j.geoderma.2020.114917
Richter M, Rosselló-Móra R (2009) Shifting the genomic gold standard for the prokaryotic species definition. Proc Natl Acad Sci U S A 106:19126–19131. https://doi.org/10.1073/pnas.0906412106
Rodriguez-R LM, Konstantinidis KT (2014) Bypassing cultivation to identify bacterial species. Microbe 9:111–118. https://doi.org/10.1128/microbe.9.111.1
Rudra B, Gupta RS (2021) Phylogenomic and comparative genomic analyses of species of the family Pseudomonadaceae: Proposals for the genera Halopseudomonas gen. nov. and Atopomonas gen. nov., merger of the genus Oblitimonas with the genus Thiopseudomonas, and transfer of some misclassified species of the genus Pseudomonas into other genera. Int J Syst Evol Microbiol 71:005011. https://doi.org/10.1099/ijsem.0.005011
Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425. https://doi.org/10.1093/oxfordjournals.molbev.a040454
Stackebrandt E, Ebers J (2006) Taxonomic parameters revisited: Tarnished gold standards. Microbiol Today 8:6–9
Suvorova IA, Ravcheev DA, Gelfand MS (2012) Regulation and evolution of malonate and propionate catabolism in proteobacteria. J Bacteriol 194:3234–3240. https://doi.org/10.1128/JB.00163-12
Tan W-B, Jiang Z, Chen C, Yuan Y, Gao L-F, Wang H-F, Cheng J, Li WJ, Wang A-J (2015) Thiopseudomonas denitrificans gen. nov., sp. nov., isolated from anaerobic activated sludge. Int J Syst Evol Microbiol 65:225–229. https://doi.org/10.1099/ijs.0.064634-0
Tatusova T, DiCuccio M, Badretdin A, Chetvernin V, Nawrocki EP, Zaslavsky L, Lomsadze A, Pruitt KD, Borodovsky M, Ostell J (2016) NCBI prokaryotic genome annotation pipeline. Nucleic Acids Res 44:6614–6624. https://doi.org/10.1093/nar/gkw569
Thompson CC, Chimetto L, Edwards RA, Swings J, Stackebrandt E, Thompson FL (2013) Microbial genomic taxonomy. BMC Genomics 14:913. https://doi.org/10.1186/1471-2164-14-913
Tindall BJ (1990) Lipid composition of Halobacterium lacusprofundi. FEMS Microbiol Lett 66:199–202. https://doi.org/10.1016/0378-1097(90)90282-U
Tindall BJ, Sikorski J, Smibert RA, Krieg NR (2007) Phenotypic characterization and the principles of comparative systematics. In: Reddy CA, Beveridge TJ, Breznak JA, Marzluf GA, Schmidt TM, Snyder LR et al (eds) Methods for general and molecular bacteriology, 3rd. American Society for Microbiology, Washington, pp 330–393
Torrents E, Eliasson R, Wolpher H, Gräslund A, Reichard P (2001) The anaerobic ribonucleotide reductase from Lactococcus lactis. Interactions between the two proteins NrdD and NrdG. J Biol Chem 276:33488–33494. https://doi.org/10.1074/jbc.M103743200
Truchon AN, Hendrich CG, Bigott AF, Dalsing BL, Allen C (2022) NorA, HmpX, and NorB cooperate to reduce NO toxicity during denitrification and plant pathogenesis in Ralstonia solanacearum. Microbiol Spectr 10:e0026422. https://doi.org/10.1128/spectrum.00264-22
van den Berg J, Galbiati H, Rasmussen A, Miller S, Poolman B (2016) On the mobility, membrane location and functionality of mechanosensitive channels in Escherichia coli. Sci Rep 6:32709. https://doi.org/10.1038/srep32709
Weisburg WG, Barns SM, Pelletier DA, Lane DJ (1991) 16S ribosomal DNA amplification for phylogenetic study. J Bacteriol 173:697–703. https://doi.org/10.1128/jb.173.2.697-703.1991
Yoon SH, Ha SM, Kwon S, Lim J, Kim Y, Seo H, Chun J (2017a) Introducing EzBioCloud: a taxonomically united database of 16S rRNA gene sequences and whole-genome assemblies. Int J Syst Evol Microbiol 67:1613–1617. https://doi.org/10.1099/ijsem.0.001755
Yoon SH, Ha SM, Lim J, Kwon S, Chun J (2017b) A large-scale evaluation of algorithms to calculate average nucleotide identity. Antonie Van Leeuwenhoek 110:1281–1286. https://doi.org/10.1007/s10482-017-0844-4
Zhang J, Liu Y-X, Guo X, Qin Y, Garrido-Oter R, Schulze-Lefert P, Bai Y (2021) High-throughput cultivation and identification of bacteria from the plant root microbiota. Nat Protoc 16:988–1012. https://doi.org/10.1038/s41596-020-00444-7
Zhang H, Liang Z, Zhao M, Ma Y, Luo Z, Li S, Xu H (2022) Metabolic engineering of Escherichia coli for ectoine production with a fermentation strategy of supplementing the amino donor. Front Bioeng Biotechnol 10:824859. https://doi.org/10.3389/fbioe.2022.824859
Acknowledgements
We were grateful to the reviewers and English native editors for helping us improve the paper.
Funding
This work was supported by the Fundamental Research Funds for the Central Universities at Beijing Forestry University (2021ZY61) and University–Industry Collaborative Education Program (202102083002).
Author information
Authors and Affiliations
Contributions
MMA and GZZ conceived the study and drafted the manuscript. YJL and XXL collected the samples. MMA and RNL performed the experiment and analyzed the data.
Corresponding author
Ethics declarations
Competing interests
The authors declare no competing interests.
Conflict of interest
The authors declare that there are no conflicts of interest.
Consent for publication
The authors approved for the publication.
Ethical approval
This article does not contain any studies with human participants or animals.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
An, M., Liang, R., Lu, Y. et al. Thiopseudomonas acetoxidans sp. nov., an aerobic acetic and butyric acids oxidizer isolated from anaerobic fermentation liquid of food waste. Antonie van Leeuwenhoek 117, 35 (2024). https://doi.org/10.1007/s10482-024-01932-6
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s10482-024-01932-6