Identification of determinants for entering into a viable but nonculturable state in Vibrio alginolyticus by Tn-seq.

Vibrio alginolyticus Cold Temperature Microbial Viability
Nutrient-limited condition Transposon insertion sequencing (Tn-seq) Viable but nonculturable (VBNC) Vibrio alginolyticus

Journal

Applied microbiology and biotechnology
ISSN: 1432-0614
Titre abrégé: Appl Microbiol Biotechnol
Pays: Germany
ID NLM: 8406612

Informations de publication

Date de publication:
Mar 2023
Historique:
received: 05 11 2022
accepted: 06 01 2023
revised: 03 01 2023
pubmed: 3 2 2023
medline: 15 3 2023
entrez: 2 2 2023
Statut: ppublish

Résumé

The viable but nonculturable (VBNC) state is a dormant state of nonsporulating bacteria that enhances survival in adverse environments. Systematic genome-wide research on the genetic basis of VBNC formation is warranted. In this study, we demonstrated that the marine bacterium Vibrio alginolyticus lost culturability but remained viable and entered into the VBNC state when exposed to low nutrient concentrations for prolonged periods of time. Using transposon-insertion sequencing (Tn-seq), we identified 635 determinants governing the formation of the VBNC state, including 322 genes with defective effects on VBNC formation and 313 genes contributing to entry into the VBNC state. Tn-seq analysis revealed that genes involved in various metabolic pathways were shown to have an inhibitory effect on VBNC formation, while genes related to chemotaxis or folate biosynthesis promoted entry into the VBNC state. Moreover, the effects of these genes on the formation of VBNC were validated with the growth of deletion mutants of eight selected genes under nutrient-limited conditions. Interestingly, fleQ and pyrI were identified as essential for entry into the VBNC state, and they affected the formation of the VBNC state independent of RpoE or ToxR regulation. Collectively, these results provide new insights into the mechanism of VBNC formation. KEY POINTS: • Vibrio alginolyticus has the ability to enter into the VBNC state under low nutrient conditions at low temperature. • The 635 determinants for entry into the VBNC state were systematically identified by transposon-insertion sequencing. • PyrI and FleQ were validated to play significant roles in the formation of the VBNC state.

Identifiants

DOI: 10.1007/s00253-023-12376-9 PMID: 36729225
pubmed: 36729225
doi: 10.1007/s00253-023-12376-9
pii: 10.1007/s00253-023-12376-9
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

1813-1827

Subventions

Organisme : The National Key Research and Development Program of China
ID : 2022YFE0101200
Organisme : National Natural Science Foundation of China
ID : 31772893
Organisme : National Natural Science Foundation of China
ID : 32102850
Organisme : China Agriculture Research System of MOF and MARA
ID : CARS-47

Informations de copyright

© 2023. The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature.

Références

Abe A, Ohashi E, Ren H, Hayashi T, Endo H (2006) Isolation of a viable but non-culturable suppression mutant of Vibrio vulnificus: role of antioxidant enzymes in surviving stationary phase and low temperatures. Fish Sci 72:656–664
doi: 10.1111/j.1444-2906.2006.01196.x
Abe A, Ohashi E, Ren H, Hayashi T, Endo H (2007) Isolation and characterization of a cold-induced nonculturable suppression mutant of Vibrio vulnificus. Microbiol Res 162:130–138
pubmed: 16520028 doi: 10.1016/j.micres.2006.01.007
Albertini MC, Accorsi A, Teodori L, Pierfelici L, Uguccioni F, Rocchi MB, Burattini S, Citterio B (2006) Use of multiparameter analysis for Vibrio alginolyticus viable but nonculturable state determination. Cytometry A 69:260–265
pubmed: 16528721 doi: 10.1002/cyto.a.20263
Almagro-Moreno S, Kim TK, Skorupski K, Taylor RK (2015) Proteolysis of virulence regulator ToxR is associated with entry of Vibrio cholerae into a dormant state. PLoS Genet 11:e1005145
pubmed: 25849031 pmcid: 4388833 doi: 10.1371/journal.pgen.1005145
Amato SM, Brynildsen MP (2015) Persister heterogeneity arising from a single metabolic stress. Curr Biol 25:2090–2098
pubmed: 26255847 doi: 10.1016/j.cub.2015.06.034
Arora SK, Ritchings BW, Almira EC, Lory S, Ramphal R (1997) A transcriptional activator, FleQ, regulates mucin adhesion and flagellar gene expression in Pseudomonas aeruginosa in a cascade manner. J Bacteriol 179:5574–5581
pubmed: 9287015 pmcid: 179431 doi: 10.1128/jb.179.17.5574-5581.1997
Asakura H, Panutdaporn N, Kawamoto K, Igimi S, Yamamoto S, Makino S (2007) Proteomic characterization of enterohemorrhagic Escherichia coli O157:H7 in the oxidation-induced viable but non-culturable state. Microbiol Immunol 51:875–881
pubmed: 17895604 doi: 10.1111/j.1348-0421.2007.tb03969.x
Ayrapetyan M, Williams TC, Oliver JD (2015) Bridging the gap between viable but non-culturable and antibiotic persistent bacteria. Trends Microbiol 23:7–13
pubmed: 25449050 doi: 10.1016/j.tim.2014.09.004
Babin BM, Bergkessel M, Sweredoski MJ, Moradian A, Hess S, Newman DK, Tirrell DA (2016) SutA is a bacterial transcription factor expressed during slow growth in Pseudomonas aeruginosa. Proc Natl Acad Sci U S A 113:597–605
doi: 10.1073/pnas.1514412113
Baffone W, Citterio B, Vittoria E, Casaroli A, Campana R, Falzano L, Donelli G (2003) Retention of virulence in viable but non-culturable halophilic Vibrio spp. Int J Food Microbiol 89:31–39
pubmed: 14580971 doi: 10.1016/S0168-1605(03)00102-8
Baker-Austin C, Oliver JD, Alam M, Ali A, Waldor MK, Qadri F, Martinez-Urtaza J (2018) Vibrio spp. infections. Nat Rev Dis Primers 4:8
pubmed: 30002421 doi: 10.1038/s41572-018-0005-8
Basta DW, Bergkessel M, Newman DK (2017) Identification of fitness determinants during energy-limited growth arrest in Pseudomonas aeruginosa. mBio 8:e01170-17
pubmed: 29184024 pmcid: 5705914 doi: 10.1128/mBio.01170-17
Ben Kahla-Nakbi A, Besbes A, Chaieb K, Rouabhia M, Bakhrouf A (2007) Survival of Vibrio alginolyticus in seawater and retention of virulence of its starved cells. Mar Environ Res 64:469–478
pubmed: 17524473 doi: 10.1016/j.marenvres.2007.04.002
Boaretti M, Lleò MM, Bonato B, Signoretto C, Canepari P (2003) Involvement of rpoS in the survival of Escherichia coli in the viable but non-culturable state. Environ Microbiol 5:986–996
pubmed: 14510852 doi: 10.1046/j.1462-2920.2003.00497.x
Brenzinger S, van der Aart LT, van Wezel GP, Lacroix JM, Glatter T, Briegel A (2019) Structural and proteomic changes in viable but non-culturable Vibrio cholerae. Front Microbiol 10:793
pubmed: 31057510 pmcid: 6479200 doi: 10.3389/fmicb.2019.00793
Cai J, Hao Y, Xu R, Zhang Y, Ma Y, Zhang Y, Wang Q (2022) Differential binding of LuxR in response to temperature gauges switches virulence gene expression in Vibrio alginolyticus. Microbiol Res 263:127114
pubmed: 35878491 doi: 10.1016/j.micres.2022.127114
Cain AK, Barquist L, Goodman AL, Paulsen IT, Parkhill J, van Opijnen T (2020) A decade of advances in transposon-insertion sequencing. Nat Rev Genet 21:526–540
pubmed: 32533119 pmcid: 7291929 doi: 10.1038/s41576-020-0244-x
Carroll BL, Liu J (2020) Structural conservation and adaptation of the bacterial flagella motor. Biomolecules 10:1492
pubmed: 33138111 pmcid: 7693769 doi: 10.3390/biom10111492
Chao MC, Pritchard JR, Zhang YJ, Rubin EJ, Livny J, Davis BM, Waldor MK (2013) High-resolution definition of the Vibrio cholerae essential gene set with hidden Markov model-based analyses of transposon-insertion sequencing data. Nucleic Acids Res 41:9033–9048
pubmed: 23901011 pmcid: 3799429 doi: 10.1093/nar/gkt654
Chao MC, Abel S, Davis BM, Waldor MK (2016) The design and analysis of transposon insertion sequencing experiments. Nat Rev Microbiol 14:119–128
pubmed: 26775926 pmcid: 5099075 doi: 10.1038/nrmicro.2015.7
Chanchal, Banerjee P, Raghav S, Goswami HN, Jain D (2021) The antiactivator FleN uses an allosteric mechanism to regulate σ
pubmed: 34669473 pmcid: 8528422 doi: 10.1126/sciadv.abj1792
Christensen-Dalsgaard M, Gerdes K (2006) Two higBA loci in the Vibrio cholerae superintegron encode mRNA cleaving enzymes and can stabilize plasmids. Mol Microbiol 62:397–411
pubmed: 17020579 doi: 10.1111/j.1365-2958.2006.05385.x
Darcan C, Ozkanca R, Idil O, Flint KP (2009) Viable but non-culturable state (VBNC) of Escherichia coli related to EnvZ under the effect of pH, starvation and osmotic stress in sea water. Pol J Microbiol 58:307–317
pubmed: 20380141
Ding Y, Song X, Yu Z (2022) Transcriptome profiles of genes related to growth and virulence potential in Vibrio alginolyticus treated with modified clay. Microbiol Res 262:127095
pubmed: 35728394 doi: 10.1016/j.micres.2022.127095
Dong K, Pan H, Yang D, Rao L, Zhao L, Wang Y, Liao X (2020) Induction, detection, formation, and resuscitation of viable but non-culturable state microorganisms. Compr Rev Food Sci 19:149–183
doi: 10.1111/1541-4337.12513
Du M, Chen J, Zhang X, Li A, Li Y (2007) Characterization and resuscitation of viable but nonculturable Vibrio alginolyticus VIB283. Arch Microbiol 188:283–288
pubmed: 17492270 doi: 10.1007/s00203-007-0246-5
García V, Stærk K, Alobaidallah MSA, Grønnemose RB, Guerra PR, Andersen TE, Olsen JE, Herrero-Fresno A (2022) Genome-wide analysis of fitness factors in uropathogenic Escherichia coli in a pig urinary tract infection model. Microbiol Res 265:127202
pubmed: 36167007 doi: 10.1016/j.micres.2022.127202
Gibson DG, Young L, Chuang RY, Venter JC, Hutchison CA 3rd, Smith HO (2009) Enzymatic assembly of DNA molecules up to several hundred kilobases. Nat Methods 6:343–345
pubmed: 19363495 doi: 10.1038/nmeth.1318
Hung WC, Jane WN, Wong HC (2013) Association of a D-alanyl-D-alanine carboxypeptidase gene with the formation of aberrantly shaped cells during the induction of viable but nonculturable Vibrio parahaemolyticus. Appl Environ Microbiol 79:7305–7312
pubmed: 24056454 pmcid: 3837741 doi: 10.1128/AEM.01723-13
Jameelah M, Dewanti-Hariyadi R, Nurjanah S (2018) Expression of rpoS, ompA and hfq genes of Cronobacter sakazakii strain Yrt2a during stress and viable but nonculturable state. Food Sci Biotechnol 27:915–920
pubmed: 30263819 pmcid: 6049694 doi: 10.1007/s10068-018-0313-5
Kibbee RJ, Örmeci B (2017) Development of a sensitive and false-positive free PMA-qPCR viability assay to quantify VBNC Escherichia coli and evaluate disinfection performance in waste water effluent. J Microbiol Methods 132:139–147
pubmed: 27932085 doi: 10.1016/j.mimet.2016.12.004
Kim GL, Hooven TA, Norambuena J, Li B, Boyd JM, Yang JH, Parker D (2021) Growth and stress tolerance comprise independent metabolic strategies critical for Staphylococcus aureus infection. mBio 12:e0081421
pubmed: 34101490 doi: 10.1128/mBio.00814-21
Kong IS, Bates TC, Hülsmann A, Hassan H, Smith BE, Oliver JD (2004) Role of catalase and oxyR in the viable but nonculturable state of Vibrio vulnificus. FEMS Microbiol Ecol 50:133–142
pubmed: 19712354 doi: 10.1016/j.femsec.2004.06.004
Langmead B, Trapnell C, Pop M, Salzberg SL (2009) Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 10:R25
pubmed: 19261174 pmcid: 2690996 doi: 10.1186/gb-2009-10-3-r25
Lee SA, Gallagher LA, Thongdee M, Staudinger BJ, Lippman S, Singh PK, Manoil C (2015) General and condition-specific essential functions of Pseudomonas aeruginosa. Proc Natl Acad Sci U S A 112:5189–5194
pubmed: 25848053 pmcid: 4413342 doi: 10.1073/pnas.1422186112
Liang W, Wang S, Yu F, Zhang L, Qi G, Liu Y, Gao S, Kan B (2003) Construction and evaluation of a safe, live, oral Vibrio cholerae vaccine candidate, IEM108. Infect Immun 71:5498–5504
pubmed: 14500467 pmcid: 201064 doi: 10.1128/IAI.71.10.5498-5504.2003
Lv Y, Xiao J, Liu Q, Wu H, Zhang Y, Wang Q (2012) Systematic mutation analysis of two-component signal transduction systems reveals EsrA-EsrB and PhoP-PhoQ as the major virulence regulators in Edwardsiella tarda. Vet Microbiol 157:190–199
pubmed: 22227416 doi: 10.1016/j.vetmic.2011.12.018
Ma LZ, Wang D, Liu Y, Zhang Z, Wozniak DJ (2022) Regulation of biofilm exopolysaccharide biosynthesis and degradation in Pseudomonas aeruginosa. Annu Rev Microbiol 76:413–433
pubmed: 35655342 doi: 10.1146/annurev-micro-041320-111355
Masmoudi S, Denis M, Maalej S (2010) Inactivation of the gene katA or sodA affects the transient entry into the viable but non-culturable response of Staphylococcus aureus in natural seawater at low temperature. Mar Pollut Bull 60:2209–2214
pubmed: 20833402 doi: 10.1016/j.marpolbul.2010.08.017
Matsuyama BY, Krasteva PV, Baraquet C, Harwood CS, Sondermann H, Navarro MV (2016) Mechanistic insights into c-di-GMP-dependent control of the biofilm regulator FleQ from Pseudomonas aeruginosa. Proc Natl Acad Sci U S A 113:E209–E218
pubmed: 26712005 doi: 10.1073/pnas.1523148113
Meng L, Alter T, Aho T, Huehn S (2015) Gene expression profiles of Vibrio parahaemolyticus in viable but non-culturable state. FEMS Microbiol Ecol 91:fiv035
pubmed: 25873464 doi: 10.1093/femsec/fiv035
Oliver JD (2005) The viable but nonculturable state in bacteria. J Microbiol 43:93–100
pubmed: 15765062
Oliver JD (2010) Recent findings on the viable but nonculturable state in pathogenic bacteria. FEMS Microbiol Rev 34:415–425
pubmed: 20059548 doi: 10.1111/j.1574-6976.2009.00200.x
Pinto D, Santos MA, Chambel L (2015) Thirty years of viable but nonculturable state research: unsolved molecular mechanisms. Crit Rev Microbiol 41:61–76
pubmed: 23848175 doi: 10.3109/1040841X.2013.794127
Postnikova OA, Shao J, Mock NM, Baker CJ, Nemchinov LG (2015) Gene expression profiling in viable but nonculturable (VBNC) cells of Pseudomonas syringae pv. syringae. Front Microbiol 6:1419
pubmed: 26733964 pmcid: 4683178 doi: 10.3389/fmicb.2015.01419
Pritchard JR, Chao MC, Abel S, Davis BM, Baranowski C, Zhang YJ, Rubin EJ, Waldor MK (2014) ARTIST: high-resolution genome-wide assessment of fitness using transposon-insertion sequencing. PLoS Genet 10:e1004782
pubmed: 25375795 pmcid: 4222735 doi: 10.1371/journal.pgen.1004782
Pu Y, Li Y, Jin X, Tian T, Ma Q, Zhao Z, Lin SY, Chen Z, Li B, Yao G, Leake MC, Lo CJ, Bai F (2019) ATP-Dependent dynamic protein aggregation regulates bacterial dormancy depth critical for antibiotic tolerance. Mol Cell 73:143–156
pubmed: 30472191 doi: 10.1016/j.molcel.2018.10.022
Ravel J, Hill RT, Colwell RR (1994) Isolation of a Vibrio cholerae transposon-mutant with an altered viable but nonculturable response. FEMS Microbiol Lett 120:57–61
pubmed: 8056295 doi: 10.1111/j.1574-6968.1994.tb07007.x
Rozen Y, Larossa RA, Templeton LJ, Smulski DR, Belkin S (2002) Gene expression analysis of the response by Escherichia coli to seawater. Antonie Van Leeuwenhoek 81:15–25
pubmed: 12448701 doi: 10.1023/A:1020500821856
Ruhal R, Kataria R (2021) Biofilm patterns in gram-positive and gram-negative bacteria. Microbiol Res 251:126829
pubmed: 34332222 doi: 10.1016/j.micres.2021.126829
Saegeman VS, De Vos R, Tebaldi ND, van der Wolf JM, Bergervoet JH, Verhaegen J, Lismont D, Verduyckt B, Ectors NL (2007) Flow cytometric viability assessment and transmission electron microscopic morphological study of bacteria in glycerol. Microsc Microanal 13:18–29
pubmed: 17234033 doi: 10.1017/S1431927607070079
Santander RD, Figàs-Segura À, Biosca EG (2018) Erwinia amylovora catalases KatA and KatG are virulence factors and delay the starvation-induced viable but non-culturable (VBNC) response. Mol Plant Pathol 19:922–934
pubmed: 28675630 doi: 10.1111/mpp.12577
Schets FM, van den Berg HH, Demeulmeester AA, van Dijk E, Rutjes SA, van Hooijdonk HJ, de Roda Husman AM (2006) Vibrio alginolyticus infections in the Netherlands after swimming in the North Sea. Euro Surveill 11(E061109):3
Shao S, Li C, Zhao L, Zhang Y, Yin K, Wang Q (2021) Interplay between ferric uptake regulator Fur and horizontally acquired virulence regulator EsrB coordinates virulence gene expression in Edwardsiella piscicida. Microbiol Res 253:126892
pubmed: 34673373 doi: 10.1016/j.micres.2021.126892
Su CP, Jane WN, Wong HC (2013) Changes of ultrastructure and stress tolerance of Vibrio parahaemolyticus upon entering viable but nonculturable state. Int J Food Microbiol 160:360–366
pubmed: 23290246 doi: 10.1016/j.ijfoodmicro.2012.11.012
Tang J, Jia J, Chen Y, Huang X, Zhang X, Zhao L, Hu W, Wang C, Lin C, Wu Z (2018) Proteomic analysis of Vibrio parahaemolyticus under cold stress. Curr Microbiol 75:20–26
pubmed: 28831596 doi: 10.1007/s00284-017-1345-4
van Opijnen T, Camilli A (2013) Transposon insertion sequencing: a new tool for systems-level analysis of microorganisms. Nat Rev Microbiol 11:435–442
pubmed: 23712350 doi: 10.1038/nrmicro3033
Vitale A, Paszti S, Takahashi K, Toyofuku M, Pessi G, Eberl L (2020) Mapping of the denitrification pathway in Burkholderia thailandensis by genome-wide mutant profiling. J Bacteriol 202:e00304-e320
pubmed: 32900830 pmcid: 7648151 doi: 10.1128/JB.00304-20
Wang HW, Chung CH, Ma TY, Wong HC (2013) Roles of alkyl hydroperoxide reductase subunit C (AhpC) in viable but nonculturable Vibrio parahaemolyticus. Appl Environ Microbiol 79:3734–3743
pubmed: 23563952 pmcid: 3675929 doi: 10.1128/AEM.00560-13
Wang S, 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 184:1630–1639
pubmed: 11872714 pmcid: 134897 doi: 10.1128/JB.184.6.1630-1639.2002
Wei L, Wu Y, Yang G, Xu R, Liu X, Liu Q, Zhang Y, Ma Y, Wang Q (2019) Genome-wide identification of fitness factors in seawater for Edwardsiella piscicida. Appl Environ Microbiol 85:e00233-e319
pubmed: 30877123 pmcid: 6498171 doi: 10.1128/AEM.00233-19
Wu B, Liang W, Yan M, Li J, Zhao H, Cui L, Zhu F, Zhu J, Kan B (2020) Quorum sensing regulation confronts the development of a viable but non-culturable state in Vibrio cholerae. Environ Microbiol 22:4314–4322
pubmed: 32319181 doi: 10.1111/1462-2920.15026
Xu T, Cao H, Zhu W, Wang M, Du Y, Yin Z, Chen M, Liu Y, Yang B, Liu B (2018) RNA-seq-based monitoring of gene expression changes of viable but non-culturable state of Vibrio cholerae induced by cold seawater. Environ Microbiol Rep 10:594–604
pubmed: 30058121 doi: 10.1111/1758-2229.12685
Yang G, Billings G, Hubbard TP, Park JS, Yin Leung K, Liu Q, Davis BM, Zhang Y, Wang Q, Waldor MK (2017) Time-resolved transposon insertion sequencing reveals genome-wide fitness dynamics during infection. mBio 8:e01581-17
pubmed: 28974620 pmcid: 5626973 doi: 10.1128/mBio.01581-17
Yin K, Guan Y, Ma R, Wei L, Liu B, Liu X, Zhou X, Ma Y, Zhang Y, Waldor MK, Wang Q (2018) Critical role for a promoter discriminator in RpoS control of virulence in Edwardsiella piscicida. PLoS Pathog 14:e1007272
pubmed: 30169545 pmcid: 6136808 doi: 10.1371/journal.ppat.1007272
Yin W, Zhang N, Xu H, Gong X, Long H, Ren W, Zhang X, Cai X, Huang A, Xie Z (2021) Stress adaptation and virulence in Vibrio alginolyticus is mediated by two (p)ppGpp synthetase genes, relA and spoT. Microbiol Res 253:126883
pubmed: 34626929 doi: 10.1016/j.micres.2021.126883
Zeng B, Zhao G, Cao X, Yang Z, Wang C, Hou L (2013) Formation and resuscitation of viable but nonculturable Salmonella typhi. Biomed Res Int 2013:907170
pubmed: 23509799 doi: 10.1155/2013/907170
Zhang N, Zhang S, Ren W, Gong X, Long H, Zhang X, Cai X, Huang A, Xie Z (2021) Roles of rpoN in biofilm formation of Vibrio alginolyticus HN08155 at different cell densities. Microbiol Res 247:126728
pubmed: 33684638 doi: 10.1016/j.micres.2021.126728
Zhao F, Wang Y, An H, Hao Y, Hu X, Liao X (2016) New insights into the formation of viable but nonculturable Escherichia coli O157:H7 induced by high-pressure CO
pubmed: 27578754 pmcid: 4999544 doi: 10.1128/mBio.00961-16
Zhao X, Zhong J, Wei C, Lin CW, Ding T (2017) Current perspectives on viable but non-culturable state in foodborne pathogens. Front Microbiol 8:580
pubmed: 28421064 pmcid: 5378802 doi: 10.3389/fmicb.2017.00580
Zhong Q, Tian J, Wang J, Fang X, Liao Z (2018) iTRAQ-based proteomic analysis of the viable but nonculturable state of Vibrio parahaemolyticus ATCC 17802 induced by food preservative and low temperature. Food Control 85:369–375
doi: 10.1016/j.foodcont.2017.10.011
Zhong Q, Wang B, Wang J, Liu Y, Fang X, Liao Z (2019) Global proteomic analysis of the resuscitation state of Vibrio parahaemolyticus compared with the normal and viable but non-culturable state. Front Microbiol 10:1045
pubmed: 31134040 pmcid: 6517545 doi: 10.3389/fmicb.2019.01045
Zhou M, Huang Y, Zhang Y, Wang Q, Ma Y, Shao S (2022) Roles of virulence regulator ToxR in viable but non-culturable formation by controlling reactive oxygen species resistance in pathogen Vibrio alginolyticus. Microbiol Res 254:126900
pubmed: 34700184 doi: 10.1016/j.micres.2021.126900

Auteurs

Jingxiao Cai (J)

State Key Laboratory of Bioreactor Engineering, Shanghai Frontiers Science Center of Optogenetic Techniques for Cell Metabolism, East China University of Science and Technology, Shanghai, 200237, China.

Mengqing Zhou (M)

State Key Laboratory of Bioreactor Engineering, Shanghai Frontiers Science Center of Optogenetic Techniques for Cell Metabolism, East China University of Science and Technology, Shanghai, 200237, China.

Yuanxing Zhang (Y)

Southern Marine Science and Engineering Guangdong Laboratory (Zhuhai), Zhuhai, 519000, China.
Shanghai Engineering Research Center of Maricultured Animal Vaccines, Shanghai, 200237, China.

Yue Ma (Y)

State Key Laboratory of Bioreactor Engineering, Shanghai Frontiers Science Center of Optogenetic Techniques for Cell Metabolism, East China University of Science and Technology, Shanghai, 200237, China. mymarine@ecust.edu.cn.
Shanghai Engineering Research Center of Maricultured Animal Vaccines, Shanghai, 200237, China. mymarine@ecust.edu.cn.
Shanghai Collaborative Innovation Center for Biomanufacturing, 130 Meilong Road, Shanghai, 200237, China. mymarine@ecust.edu.cn.

Yibei Zhang (Y)

State Key Laboratory of Bioreactor Engineering, Shanghai Frontiers Science Center of Optogenetic Techniques for Cell Metabolism, East China University of Science and Technology, Shanghai, 200237, China. ybzhang@ecust.edu.cn.
Shanghai Engineering Research Center of Maricultured Animal Vaccines, Shanghai, 200237, China. ybzhang@ecust.edu.cn.
ORCID: 0000-0001-8706-0951

Qiyao Wang (Q)

State Key Laboratory of Bioreactor Engineering, Shanghai Frontiers Science Center of Optogenetic Techniques for Cell Metabolism, East China University of Science and Technology, Shanghai, 200237, China.
Shanghai Engineering Research Center of Maricultured Animal Vaccines, Shanghai, 200237, China.
Shanghai Collaborative Innovation Center for Biomanufacturing, 130 Meilong Road, Shanghai, 200237, China.

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Classifications MeSH

questionsmedicales.fr › Bactéries › Proteobacteria › Gammaproteobacteria › Vibrionaceae › Vibrio › Vibrio alginolyticus › Identification of determinants for entering...
questionsmedicales.fr › Environnement et santé publique › Environnement › Concepts météorologiques › Atmosphère › Temps (météorologie) › Température › Basse température › Identification of determinants for entering...
questionsmedicales.fr › Phénomènes microbiologiques › Viabilité microbienne › Identification of determinants for entering...