Skip to main content
SpringerLink
Log in

Comprehensive insights into the metabolism characteristics of small RNA Qrr4 in Vibrio alginolyticus

  • Applied Microbial and Cell Physiology
  • Published:
Applied Microbiology and Biotechnology Aims and scope Submit manuscript

Abstract

Vibrio alginolyticus is an important foodborne pathogen that can infect both humans and marine animals and cause massive economic losses in aquaculture. Small noncoding RNAs (sRNAs) are emerging posttranscriptional regulators that affect bacterial physiology and pathological processes. In the present work, a new cell density-dependent sRNA, Qrr4, was characterized in V. alginolyticus based on a previously reported RNA-seq analysis and bioinformatics approach. The effects of Qrr4 actions on the physiology, virulence, and metabolism of V. alginolyticus were comprehensively investigated based on molecular biology and metabolomics approaches. The results showed that qrr4 deletion markedly inhibited growth, motility and extracellular protease activities. Additionally, nontargeted metabolism and lipidomics analyses revealed that qrr4 deletion induced significant disturbance of multiple metabolic pathways. The key metabolic remodelling that occurred in response to qrr4 deletion was found to involve phospholipid, nucleotide, carbohydrate and amino acid metabolic pathways, providing novel clues about a potential mechanism via which mutation of qrr4 could interfere with cellular energy homeostasis, modulate membrane phospholipid composition and inhibit nucleic acid and protein syntheses to regulate the motility, growth and virulence characteristics of V. alginolyticus. Overall, this study provides a comprehensive understanding of the regulatory roles of the new cell density-dependent sRNA Qrr4 in V. alginolyticus.

Key points

• A novel cell density-dependent sRNA, Qrr4, was cloned in V. alginolyticus.

•Qrr4 regulated growth and virulence factors of V. alginolyticus.

• Phospholipid, nucleotide and energy metabolisms were modulated obviously by Qrr4.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Data availability

All data generated or analysed during this study are included in this published article (and its supplementary information files).

References

  • Adnan M, Morton G, Hadi S (2011) Analysis of rpoS and bolA gene expression under various stress-induced environments in planktonic and biofilm phase using 2-ΔΔCT method. Mol Cell Biochem 357(1-2):275–282

    Article  CAS  PubMed  Google Scholar 

  • Afzal M, Kuipers OP, Shafeeq S (2017) Niacin-mediated gene expression and role of NiaR as a transcriptional repressor of niaX, nadC, and pnuC in Streptococcus pneumoniae. Front Cell Infect Microbiol 7:70

    Article  PubMed  PubMed Central  Google Scholar 

  • Alvarez-Eraso KL, Muñoz-Martínez LM, Alzate JF, Barrera LF, Baena A (2022) Modulatory impact of the sRNA Mcr11 in two clinical isolates of Mycobacterium tuberculosis. Curr Microbiol 79:39

    Article  CAS  PubMed  Google Scholar 

  • Austin B (2010) Vibrios as causal agents of zoonoses. Vet Microbiol 140(3-4):310–317

    Article  CAS  PubMed  Google Scholar 

  • Behrens S, Widder S, Mannala GK, Qing X, Madhugiri R, Kefer N, Mraheil MA, Rattei T, Hain T (2014) Ultra deep sequencing of Listeria monocytogenes sRNA transcriptome revealed new antisense RNAs. PLoS One 9(2):e83979

    Article  PubMed  PubMed Central  Google Scholar 

  • Boiteux S (1993) Properties and biological functions of the NTH and FPG proteins of Escherichia coli: two DNA glycosylases that repair oxidative damage in DNA. J Photochem Photobiol B 19(2):87–96

    Article  CAS  PubMed  Google Scholar 

  • Caswell CC, Oglesby-Sherrouse AG, Murphy ER (2014) Sibling rivalry: related bacterial small RNAs and their redundant and non-redundant roles. Front Cell Infect Microbiol 4:151

    Article  PubMed  PubMed Central  Google Scholar 

  • Davis BJ, Corrigan AE, Sun Z, Atherly E, Curriero FC (2021) A case-control analysis of traceback investigations for Vibrio parahaemolyticus infections (vibriosis) and pre-harvest environmental conditions in Washington State, 2013–2018. Sci Total Environ 752:141650

    Article  CAS  PubMed  Google Scholar 

  • Deng YQ, Chen C, Zhao Z, Zhao JJ, Jacq A, Huang XH, Yang YY (2016) The RNA chaperone Hfq is involved in colony morphology, nutrient utilization and oxidative and envelope stress response in Vibrio alginolyticus. PLoS One 11(9):e0163689

    Article  PubMed  PubMed Central  Google Scholar 

  • Deng YQ, Su YL, Liu SL, Guo ZX, Cheng CH, Ma HL, Wu JJ, Feng J, Chen C (2018) Identification of a novel small RNA srvg23535 in Vibrio alginolyticus ZJ-T and its characterization with phenotype microarray technology. Front Microbiol 9:2394

    Article  PubMed  PubMed Central  Google Scholar 

  • Dutta T, Srivastava S (2018) Small RNA-mediated regulation in bacteria: a growing palette of diverse mechanisms. Gene 656:60–72

    Article  CAS  PubMed  Google Scholar 

  • Echazarreta MA, Klose KE (2019) Vibrio flagellar synthesis. Front Cell Infect Microbiol 9:131

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Eisenbart SK, Alzheimer M, Pernitzsch SR, Dietrich S, Sharma CM (2020) A repeat-associated small RNA controls the major virulence factors of Helicobacter pylori. Mol Cell 80(2):210–226

    Article  CAS  PubMed  Google Scholar 

  • Feng LH, Rutherford ST, Papenfort K, Bagert JD, van Kessel JC, Tirrell DA, Wingreen NS, Bassler BL (2015) A Qrr noncoding RNA deploys four different regulatory mechanisms to optimize quorum-sensing dynamics. Cell 160:228–240

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Franco TA, Hegde S, Blanchard JS (2016) Chemical mechanism of the branched-chain aminotransferase IlvE from Mycobacterium tuberculosis. Biochemistry 55(45):6295–6303

    Article  Google Scholar 

  • Gong QY, Yang MJ, Yang LF, Chen ZG, Jiang M, Peng B (2020) Metabolic modulation of redox state confounds fish survival against Vibrio alginolyticus infection. Microb Biotechnol 13(3):796–812

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guzman LM, Belin D, Carson MJ, Beckwith J (1995) Tight regulation, modulation, and high-level expression by vectors containing the arabinose PBAD promoter. J Bacteriol 177(14):4121–4130

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Han XL (2016) Lipidomics for studying metabolism. Nat Rev Endocrinol 12(11):668–679

    Article  CAS  PubMed  Google Scholar 

  • Hawver LA, Giulietti JM, Baleja JD, Ng WL (2016) Quorum sensing coordinates cooperative expression of pyruvate metabolism genes to maintain a sustainable environment for population stability. mBio 7(6):e01863–e01816

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huang LX, Hu J, Su YQ, Qin YG, Kong WD, Ma Y, Xu XJ, Lin M, Yan QP (2015) Identification and characterization of three Vibrio alginolyticus non-coding RNAs involved in adhesion, chemotaxis, and motility processes. Front Cell Infect Microbiol 5:56

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hunter GA, Keener JP (2014) Mechanisms underlying the additive and redundant Qrr phenotypes in Vibrio harveyi and Vibrio cholerae. J Theor Biol 340:38–49

    Article  CAS  PubMed  Google Scholar 

  • Ishikawa Y, Cassan C, Kadeer A, Yuasa K, Sato N, Sonoike K, Kaneko Y, Miyagi A, Takahashi H, Ishikawa T, Yamaguchi M, Nishiyama Y, Hihara Y, Gibon Y, Kawai-Yamada M (2021) The NAD kinase Slr0400 functions as a growth repressor in Synechocystis sp. PCC 6803. Plant Cell Physiol 62(4):668–677

    Article  CAS  PubMed  Google Scholar 

  • Jiang M, Yang LF, Chen ZG, Lai SS, Zheng J, Peng B (2020) Exogenous maltose enhances Zebrafish immunity to levofloxacin-resistant Vibrio alginolyticus. Microb Biotechnol 13(4):1213–1227

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kaiser JC, Heinrichs DE (2018) Branching out: alterations in bacterial physiology and virulence due to branched-chain amino acid deprivation. mBio 9(5):e01188–e01118

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kasai H (1997) Analysis of a form of oxidative DNA damage, 8-hydroxy-2'-deoxyguanosine, as a marker of cellular oxidative stress during carcinogenesis. Mutat Res 387(3):147–163

    Article  CAS  PubMed  Google Scholar 

  • Keersmaecker S, Sonck K, Vanderleyden J (2006) Let LuxS speak up in AI-2 signaling. Trends Microbiol 14(3):114–119

    Article  PubMed  Google Scholar 

  • Lee KK, Chen FR, Yu SR, Yang TI, Liu PC (1997) Effects of extracellular products of Vibrio alginolyticus on penaeid prawn plasma components. Lett Appl Microbiol 25(2):98–100

    Article  CAS  PubMed  Google Scholar 

  • Li YH, Yan JX, Guo XQ, Wang XC, Liu FX, Cao YB (2022) The global regulators ArcA and CytR collaboratively modulate Vibrio cholerae motility. BMC Microbiol 22(1):22

    Article  PubMed  PubMed Central  Google Scholar 

  • Liu Q, Wang PB, Ma Y, Zhang YX (2007) Characterization of the Vibrio alginolyticus fur gene and localization of essential amino acid sites in Fur by site-directed mutagenesis. J Mol Microbiol Biotechnol 13(1-3):15–21

    CAS  PubMed  Google Scholar 

  • Liu H, Liu W, He XX, Chen XF, Yang JF, Wang Y, Li Y, Ren JM, Xu WS, Zhao YN (2020) Characterization of a cell density-dependent sRNA, Qrr, and its roles in the regulation of the quorum sensing and metabolism in Vibrio alginolyticus. Appl Microbiol Biotechnol 104(4):1707–1720

    Article  CAS  PubMed  Google Scholar 

  • Lu P, Zhang Y, Hu YB, Francis M S, Chen SY (2014) A cis-encoded sRNA controls the expression of fabH2 in Yersinia. FEBS Lett 588:1961–1966

    Article  CAS  PubMed  Google Scholar 

  • Martin M, Wright PR, Rolf B (2017) IntaRNA 2.0: enhanced and customizable prediction of RNA–RNA interactions. Nucleic Acids Res 45:W435–W439

    Article  Google Scholar 

  • Melson EM, Kendall MM (2019) The sRNA DicF integrates oxygen sensing to enhance enterohemorrhagic Escherichia coli virulence via distinctive RNA control mechanisms. Proc Natl Acad Sci USA 116(28):14210–14215

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mey AR, Craig SA, Payne SM (2005) Characterization of Vibrio cholerae RyhB: the RyhB regulon and role of ryhB in biofilm formation. Infect Immun 73(9):5706–5719

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moolla N, Goosens VJ, Kana BD, Gordhan BG (2014) The contribution of Nth and Nei DNA glycosylases to mutagenesis in Mycobacterium smegmatis. DNA Repair 13:32–41

    Article  CAS  PubMed  Google Scholar 

  • Naz S, Vallejo M, Garcia A, Barbas C (2014) Method validation strategies involved in non-targeted metabolomics. J Chromatogr A 1353:99–105

    Article  CAS  PubMed  Google Scholar 

  • Nguyen AN, Jacq A (2014) Small RNAs in the Vibrionaceae: an ocean still to be explored. Wiley Interdiscip Rev RNA 5(3):381–392

    Article  CAS  PubMed  Google Scholar 

  • Nicholson JK, Lindon JC, Holmes E (1999) ‘Metabonomics’: understanding the metabolic responses of living systems to pathophysiological stimuli via multivariate statistical analysis of biological NMR spectroscopic data. Xenobiotica 29(11):1181–1189

    Article  CAS  PubMed  Google Scholar 

  • Okabe M, Yakushi T, Homma M (2005) Interactions of MotX with MotY and with the PomA/PomB sodium ion channel complex of the Vibrio alginolyticus polar flagellum. J Biol Chem 280(27):25659–25664

    Article  CAS  PubMed  Google Scholar 

  • Rui HP, Liu Q, Ma Y, Wang QY, Zhang YX (2010) Roles of LuxR in regulating extracellular alkaline serine protease A, extracellular polysaccharide and mobility of Vibrio alginolyticus. FEMS Microbiol Lett 285(2):155–162

    Article  Google Scholar 

  • Rustam YH, Reid GE (2018) Analytical challenges and recent advances in mass spectrometry based lipidomics. Anal Chem 90(1):374–397

    Article  CAS  PubMed  Google Scholar 

  • Rutherford ST, Kessel JC, Shao Y, Bassler BL (2011) AphA and LuxR/HapR reciprocally control quorum sensing in vibrios. Genes Dev 25(4):397–408

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rutherford ST, Valastyan JS, Taillefumier T, Wingreen NS, Bassler BL (2015) Comprehensive analysis reveals how single nucleotides contribute to noncoding RNA function in bacterial quorum sensing. Proc Natl Acad Sci USA 112(44):e6038–e6047

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sabharwal D, Song T, Papenfort K, Wai SN (2015) The VrrA sRNA controls a stationary phase survival factor Vrp of Vibrio cholerae. RNA Biol 12(2):186–196

    Article  PubMed  PubMed Central  Google Scholar 

  • Seong HJ, Han SW, Sul WJ (2021) Prokaryotic DNA methylation and its functional roles. J Microbiol 59(3):242–248

    Article  CAS  PubMed  Google Scholar 

  • Shanbhag K, Mhetre A, Khandelwal N, Kamat SS (2020) The lysophosphatidylserines-an emerging class of signalling lysophospholipids. J Membr Biol 253(5):381–397

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shao Y, Bassler BL (2014) Quorum regulatory small RNAs repress type VI secretion in Vibrio cholerae. Mol Microbiol 92(5):921–930

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shigenaga MK, Ames BN (1991) Assays for 8-hydroxy-2'-deoxyguanosine: a biomarker of in vivo oxidative DNA damage. Free Radic Biol Med 10(3-4):211–216

    Article  CAS  PubMed  Google Scholar 

  • Steiner T, Zachary M, Bauer S, Müller MJ, Krischke M, Radziej S, Klepsch M, Huettel B, Eisenreich W, Rudel T, Beier D (2023) Central role of sibling small RNAs NgncR_162 and NgncR_163 in main metabolic pathways of Neisseria gonorrhoeae. mBio 4:e0309322

    Article  Google Scholar 

  • Stephan K, Paul B, Wright PR, Atilho RM, Brewer KI, Martin H, Breaker RR, Hess WR (2018) A glutamine riboswitch is a key element for the regulation of glutamine synthetase in cyanobacteria. Nucleic Acids Res 46(19):10082–10094

    Google Scholar 

  • Storz G, Altuvia S, Wassarman KM (2005) An abundance of RNA regulators. Annu Rev Biochem 74:199–217

    Article  CAS  PubMed  Google Scholar 

  • Tague JG, Hong J, Kalburge SS, Boyd EF (2022) Regulatory small RNA Qrr2 is expressed independently of sigma factor-54 and can function as the sole Qrr small RNA to control quorum sensing in Vibrio parahaemolyticus. J Bacteriol 204(1):e00350–e00321

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Teschler JK, Zamorano D, Utada AS, Warner CJ, Wong GC, Linington RG, Yildiz FH (2015) Living in the matrix: assembly and control of Vibrio cholerae biofilms. Nat Rev Microbiol 13(5):255–268

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tian Y, Wang QY, Liu Q, Ma Y, Cao XD, Zhang YX (2008) Role of RpoS in stress survival, synthesis of extracellular autoinducer 2, and virulence in Vibrio alginolyticus. Arch Microbiol 190(5):585–594

    Article  CAS  PubMed  Google Scholar 

  • Toledo-Arana A, Repoila F, Cossart P (2007) Small noncoding RNAs controlling pathogenesis. Curr Opin Microbiol 10(2):182–188

    Article  CAS  PubMed  Google Scholar 

  • Vogel J, Bartels V, Tang TH, Churakov G, Slagter-Jager JG, Hüttenhofer A, Wagner EG (2003) RNomics in Escherichia coli detects new sRNA species and indicates parallel transcriptional output in bacteria. Nucleic Acids Res 31(22):6435–6443

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang SY, Lauritz J, Jass J, Milton DL (2002) A ToxR homolog from Vibrio anguillarum serotype O1 regulates its own production, bile resistance, and biofilm formation. J Bacteriol 184(6):1630–1639

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Watve S, Thomas J, Hammer B (2015) CytR is a global positive regulator of competence, type VI secretion, and chitinases in Vibrio cholerae. PLoS One 10(9):e0138834

    Article  PubMed  PubMed Central  Google Scholar 

  • Xi DY, Yang S, Liu Q, Li YJ, Li YH, Yan JX, Wang XC, Ning KX, Cao BY (2020) The response regulator ArcA enhances biofilm formation in the vpsT manner under the anaerobic condition in Vibrio cholerae. Microb Pathog 144:104197

    Article  CAS  PubMed  Google Scholar 

  • Yan D, Ikeda TP, Shauger AE (1996) Glutamate is required to maintain the steady-state potassium pool in Salmonella typhimurium. Proc Natl Acad Sci USA 93(13):6527–6531

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang MJ, Cheng ZX, Jiang M, Zeng ZH, Peng B, Peng XX, Li H (2018) Boosted TCA cycle enhances survival of zebrafish to Vibrio alginolyticus infection. Virulence 9(1):634–644

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang MJ, Xu D, Yang DX, Li L, Peng XX, Chen ZG, Li H (2020) Malate enhances survival of zebrafish against Vibrio alginolyticus infection in the same manner as taurine. Virulence 11(1):349–364

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yin Y, Yin YP, Yang H, Chen ZG, Zheng J, Peng B (2022) Vibrio alginolyticus survives from ofloxacin stress by metabolic adjustment. Front Microbiol 13:818923

    Article  PubMed  PubMed Central  Google Scholar 

  • Zakataeva NP (2021) Microbial 5'-nucleotidases: their characteristics, roles in cellular metabolism, and possible practical applications. Appl Microbiol Biotechnol 105(20):7661–7681

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zha F, Pang R, Huang SX, Zhang JM, Wang J, Chen MT, Xue L, Ye QG, Wu S, Yang MY, Gu QH, Ding Y, Zhang H, Wu QP (2022) Gene regulatory network of the noncoding RNA Qrr5 involved in the cytotoxicity of Vibrio parahaemolyticus during infection. Microorganisms 10:2084

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao XN, Koestler BJ, Waters CM, Hammer BK (2013) Post-transcriptional activation of a diguanylate cyclase by quorum sensing small RNAs promotes biofilm formation in Vibrio cholerae. Mol Microbiol 89(5):989–1002

    Article  CAS  PubMed  Google Scholar 

  • Zhao YN, Zhao CX, Li YL, Chang YW, Zhang JJ, Zeng ZD, Lu X, Xu GW (2014) Study of metabolite differences of flue-cured tobacco from different regions using a pseudotargeted gas chromatography with mass spectrometry selected-ion monitoring method. J Sep Sci 37(16):2177–2184

    Article  CAS  PubMed  Google Scholar 

  • Zhao YN, Ren JM, Jiang HY, Chen XF, Xu MD, Li Y, Zhao JY, Chen D, Zhang K, Li H, Liu H (2021) Metabolomics and lipidomics analyses delineating Hfq deletion-induced metabolic alterations in Vibrio alginolyticus. Aquaculture 535:736349

    Article  CAS  Google Scholar 

  • Zheng L, Lin YB, Lu S, Zhang JZ, Bogdanov M (2017) Biogenesis, transport and remodeling of lysophospholipids in Gram-negative bacteria. Biochim Biophys Acta Mol Cell Biol Lipids 1862(11):1404–1413

    Article  CAS  PubMed  Google Scholar 

  • Zuker M (2003) Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res 31(13):3406–3415

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We thank Qinfeng Xu for technical assistance.

Funding

This research was supported by the foundations (Nos. 31800328, and 32070129) from the National Natural Science Foundation of China, Key Research Project of Shaanxi Provincial Science and Technology Department (No.2021NY-164, and 2023-YBNY-171), Young Talent Fund of University Association for Science and Technology of Shaanxi (No.20210213), Xi’an Science and Technology Project (22NYYF036), Hebei Province Natural Science Foundation (B2019415024), Hebei Province Scientific Research Key Projects of Education Department (ZD2021038) and Key Research and Development Program of Hebei Province under Grant (20373902D).

Author information

Authors and Affiliations

  1. School of Food and Biological Engineering, Shaanxi University of Science & Technology, Xi’an, 710021, China

    Yanni Zhao, Ningning Zhou, Jiamin Ren, Wang Liu, Chuang Zhou, Xuefeng Chen, Juanjuan Cao, Jinfang Yang, Jie Han & Huan Liu

  2. School of Environmental Engineering, Hebei University of Environmental Engineering, Qinhuangdao, 066102, China

    Jieyu Zhao

Authors
  1. Yanni Zhao
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ningning Zhou
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jiamin Ren
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Wang Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Chuang Zhou
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Xuefeng Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Jieyu Zhao
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Juanjuan Cao
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Jinfang Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Jie Han
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Huan Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

YNZ and HL conceived and designed the study. NNZ, JMR and WL performed the experiments and analysed the data. CZ, JYZ, JJC, JFY and JH provided expertise and analysis support. HL guided the whole manuscript writing. YNZ and NNZ wrote the manuscript. XFC corrected the manuscript. All authors read and approved the manuscript.

Corresponding author

Correspondence to Huan Liu.

Ethics declarations

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Conflict of interest

The authors declare no competing interests.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

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.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhao, Y., Zhou, N., Ren, J. et al. Comprehensive insights into the metabolism characteristics of small RNA Qrr4 in Vibrio alginolyticus. Appl Microbiol Biotechnol 107, 1887–1902 (2023). https://doi.org/10.1007/s00253-023-12435-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00253-023-12435-1

Keywords

Search

Navigation