Skip to main content
SpringerLink
Log in

Transcriptional responses to starvation of pathogenic Vibrio harveyi strain DY1

  • Aquaculture and Fisheries
  • Published:
Journal of Oceanology and Limnology Aims and scope Submit manuscript

Abstract

Vibrio harveyi is a pathogen of various aquatic organisms that has been recently associated with massive mortality episodes in the aquaculture industry. Recurrent outbreaks of vibriosis are closely correlated with the capacity of this bacterial species to survive long-term starvation conditions. To study the regulation mechanism of gene expression at the transcriptional level in V. harveyi under starvation conditions, the transcriptomic response profiles were determined of the Portunus trituberculatus pathogen V. harveyi strain DY1 under normal conditions and after four weeks of starvation. A total of 4 679 and 4 661 genes were expressed in the non-starved and starved cells, respectively. The significantly differentially expressed genes (DEGs) between non-starved and starved groups were identified, in which 255 genes were up-regulated and 411 genes were down-regulated. GO analysis and KEGG enrichment analysis were used to analyze the DEGs and revealed the involvement of these DEGs in many pathways, including ABC transporters, flagellum assembly, and fatty acid metabolism. Several DEGs were randomly selected and their expression levels were confirmed by quantitative real-time PCR (qRT-PCR). This is the first comprehensive transcriptomic analysis of starvation effects in V. harveyi. Our findings will facilitate future study on stress adaptation and survival mechanisms of V. harveyi.

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

Similar content being viewed by others

Data Availability Statement

All sequence data that support the findings of this study have been deposited in the NCBI Short Read. The sequence read archive (SRA) accession number: PRJNA507871.

References

  • Alcaide E, Gil-Sanz C, Sanjuán E, Esteve D, Amaro C, Silveira L. 2010. Vibrio harveyi causes disease in seahorse, Hippocampus sp. Journal of Fish Diseases, 24(5): 311–313.

    Google Scholar 

  • Arias C R, LaFrentz S, Cai W L, Olivares-Fuster O. 2012. Adaptive response to starvation in the fish pathogen flavobacterium columnare: cell viability and ultrastructural changes. BMC Microbiology, 12: 266.

    Google Scholar 

  • Austin B, Zhang X H. 2006. Vibrio harveyi: a significant pathogen of marine vertebrates and invertebrates. Letters in Applied Microbiology, 43(2): 119–124.

    Google Scholar 

  • Austin B. 2010. Vibrios as causal agents of zoonoses. Veterinary Microbiology, 140(3–4): 310–317.

    Google Scholar 

  • Biosca E G, Amaro C, Marco-Noales E, Oliver J D. 1996. Effect of low temperature on starvation-survival of the eel pathogen Vibrio vulnificus biotype 2. Applied and Environmental Microbiology, 62(2): 450–455.

    Google Scholar 

  • Company R, Sitj-Bobadilla A, Pujalte M J, Garay E, Alvarez-Pellitero P. 1999. Bacterial and parasitic pathogens in cultured common dentex, Dentex dentex L. Journal of Fish Diseases, 22(4): 299–309.

    Google Scholar 

  • Diggles B K, Moss G A, Carson J, Anderson C D. 2000. Luminous vibriosis in rock lobster Jasus verreauxi (Decapoda: Palinuridae) phyllosoma larvae associated with infection by Vibrio harveyi. Diseases of Aquatic Organisms, 43(2): 127–137.

    Google Scholar 

  • Gauger E, Smolowitz R, Uhlinger K, Casey J, Gómez-Chiarri M. 2006. Vibrio harveyi and other bacterial pathogens in cultured summer flounder, Paralichthys dentatus. Aquaculture, 260(1–4): 10–20.

    Google Scholar 

  • Haldar S, Maharajan A, Chatterjee S, Hunter S A, Chowdhury N, Hinenoya A, Asakura M, Yamasaki S. 2010. Identification of Vibrio harveyi as a causative bacterium for a tail rot disease of sea bream Sparus aurata from research hatchery in Malta. Microbiological Research, 165(8): 639–648.

    Google Scholar 

  • Higgins C F. 2001. ABC transporters: physiology, structure and mechanism—an overview. Research in Microbiology, 152(3–4): 205–210.

    Google Scholar 

  • Hispano C, Nebra Y, Blanch A R. 1997. Isolation of Vibrio harveyi from an ocular lesion in the short sunfish (Mola mola). Bulletin of the European Association of Fish Pathologists, 17(3–4): 104–107.

    Google Scholar 

  • Jiang X, Chai T J. 1996. Survival of Vibrio parahaemolyticus at low temperatures under starvation conditions and subsequent resuscitation of viable, nonculturable cells. Applied and Environmental Microbiology, 62(4): 1 300–1 305.

    Google Scholar 

  • Johnson F H, Shunk I V. 1936. An interesting new species of luminous bacteria. Journal of Bacteriology, 31(6): 585–593.

    Google Scholar 

  • Kaberdin V R, Bläsi U. 2006. Translation initiation and the fate of bacterial mRNAs. FEMS Microbiology Reviews, 30(6): 967–979.

    Google Scholar 

  • Kaberdin V R, Montánchez I, Parada C, Orruño M, Arana I, Barcina I. 2015. Unveiling the metabolic pathways associated with the adaptive reduction of cell size during vibrio harveyi persistence in seawater microcosms. Microbial Ecology, 70(3): 689–700.

    Google Scholar 

  • Kim C, Mwangi M, Chung M, Milheirço C, De Lencastre H, Tomasz A. 2013. The mechanism of heterogeneous beta-lactam resistance in MRSA: key role of the stringent stress response. PLoS One, 8(12): e82814.

    Google Scholar 

  • Kjellerberg S, Humphrey B A, Marshall K C. 1983. Initial phases of starvation and activity of bacteria at surfaces. Applied and Environmental Microbiology, 46(5): 978–984.

    Google Scholar 

  • Kraxberger-Beatty T, McGarey D J, Grier H J, Lim D V. 1990. Vibrio harveyi, an opportunistic pathogen of common snook, Centropomus undecimalis (Bloch), held in captivity. Journal of Fish Diseases, 13(6): 557–560.

    Google Scholar 

  • Kunttu H M T, Valtonen E T, Jokinen E I, Suomalainen L R. 2009. Saprophytism of a fish pathogen as a transmission strategy. Epidemics, 1(2): 96–100.

    Google Scholar 

  • Lavilla-Pitogo C R, Baticados M C L, Cruz-Lacierda E R, de la Pena L D. 1990. Occurrence of luminous bacterial disease of Penaeus monodon larvae in the Philippines. Aquaculture, 91(1–2): 1–13.

    Google Scholar 

  • Li R Q, Yu C, Li Y R, Lam T W, Yiu S M, Kristiansen K, Wang J. 2009. SOAP2: an improved ultrafast tool for short read alignment. Bioinformatics, 25(15): 1 966–1 967.

    Google Scholar 

  • Liu P C, Lee K K, Yii K C, Kou G H, Chen S N. 1996. News & Notes: isolation of Vibrio harveyi from diseased kuruma prawns Penaeus japonicus. Current Microbiology, 33(2): 129–132.

    Google Scholar 

  • McDougald D, Rice S A, Weichart D, Kjelleberg S. 1998. Nonculturability: adaptation or debilitation? FEMS Microbiology Ecology, 25(1): 1–9.

    Google Scholar 

  • Montánchez I, Arana I, Parada C, Garaizabal I, Orruño M, Barcina I, Kaberdin V R. 2014. Reprogramming of Vibrio harveyi gene expression during adaptation in cold seawater. FEMS Microbiology Ecology, 87(1): 193–203.

    Google Scholar 

  • Montánchez I, Ogayar E, Plágaro A H, Esteve-Codina A, Gómez-Garrido J, Orruño M, Arana I, Kaberdin V R. 2019. Analysis of Vibrio harveyi adaptation in sea water microcosms at elevated temperature provides insights into the putative mechanisms of its persistence and spread in the time of global warming. Scientific Reports, 9(1): 289.

    Google Scholar 

  • Mortazavi A, Williams B A, McCue K, Schaeffer L, Wold B. 2008. Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nature Methods, 5(7): 621–628.

    Google Scholar 

  • Novitsky JA, Morita R Y. 1976. Morphological characterization of small cells resulting from nutrient starvation of a psychrophilic marine vibrio. Applied and Environmental Microbiolog, 32(4): 617–622.

    Google Scholar 

  • Ortigosa M, Garay E, Pujalte M J. 1994. Numerical taxonomy of Vibrionaceae isolated from oysters and seawater along an annual cycle. Systematic and Applied Microbiology, 17(2): 216–225.

    Google Scholar 

  • Parada C, Orruño M, Kaberdin V, Bravo Z, Barcina I, Arana I. 2016. Changes in the Vibrio harveyi cell envelope subproteome during permanence in cold seawater. Microbial Ecology, 72(3): 549–558.

    Google Scholar 

  • Poindexter J S. 1981. Oligotrophy: fast and famine existence. In: Alexander M ed. Advances in Microbial Ecology. Springer, Boston, MA. p.63–89.

    Google Scholar 

  • Pujalte M J, Sitjà-Bobadilla A, Macián M C, Belloch C, Álvarez-Pellitero P, Pérez-Sánchez J, Uruburu F, Garay E. 2003. Virulence and molecular typing of Vibrio harveyi strains isolated from cultured dentex, gilthead sea bream and European sea bass. Systematic and Applied Microbiology, 26(2): 284–292.

    Google Scholar 

  • Saeed M O. 1995. Association of Vibrio harveyi with mortalities in cultured marine fish in Kuwait. Aquaculture, 136(1–2): 21–29.

    Google Scholar 

  • Sun J J, Gao X J, Qun J, Du X D, Bi K R, Zhang X J, Lin L. 2016. Comparative analysis of the survival and gene expression of pathogenic strains Vibrio harveyi after starvation. FEMS Microbiology Letters, 363(22): fnw250, https://doi.org/10.1093/femsle/fnw250.

    Google Scholar 

  • Suzina N E, Mulyukin A L, Kozlova A N, Shorokhova A P, Dmitriev V V, Barinova E S, Mokhova O N, El’-Registan G I, Duda V I. 2004. Ultrastructure of resting cells of some non-spore-forming bacteria. Microbiology, 73(4): 435–447.

    Google Scholar 

  • Svensson S L, Pryjma M, Gaynor E C. 2014. Flagella-mediated adhesion and extracellular DNA release contribute to biofilm formation and stress tolerance of Campylobacter jejuni. PLoS One, 9(8): e106063.

    Google Scholar 

  • Vatsos I N, Thompson K D, Adams A. 2003. Starvation of Flavobacterium psychrophilum in broth, stream water and distilled water. Diseases of Aquatic Organisms, 56(2): 115–126.

    Google Scholar 

  • Wai S N, Mizunoe Y, Yoshida S I. 1999. How Vibrio cholerae survive during starvation. FEMS Microbiology Letters, 180(2): 123–131.

    Google Scholar 

  • Wolf P W, Oliver J D. 1992. Temperature effects on the viable but non-culturable state of Vibrio vulnificus. FEMS Microbiology Letters, 101(1): 33–39.

    Google Scholar 

  • Zhang X H, Austin B. 2000. Pathogenicity of Vibrio harveyi to salmonids. Journal of Fish Diseases, 23(2): 93–102.

    Google Scholar 

  • Zhang X J, Bai X S, Yan B L, Bi K R, Qin L. 2014. Vibrio harveyi as a causative agent of mass mortalities of megalopa in the seed production of swimming crab Portunus trituberculatus. Aquaculture International, 22(2): 661–672

    Google Scholar 

  • Zorrilla I, Arijo S, Chabrillon M, Diaz P, Martinez-Manzanares E, Balebona M C, Moriñigo M A. 2003. Vibrio species isolated from diseased farmed sole, Solea senegalensis (Kaup), and evaluation of the potential virulence role of their extracellular products. Journal of Fish Diseases, 26(2): 103–108.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. College of Animal Science and Technology, Yangzhou University, Yangzhou, 225009, China

    Xiaodan Liu, Xiaojian Gao, Nan Chen, Yingying Zhang, Xixi Li, Yue Zhang & Xiaojun Zhang

Authors
  1. Xiaodan Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Xiaojian Gao
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Nan Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yingying Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Xixi Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Yue Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Xiaojun Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Xiaojun Zhang.

Additional information

Supported by the Jiangsu Agricultural Industry Technology System (No. 02), the National Natural Science Foundation of China (No. 31972830), the Natural Science Foundation of Jiangsu Province (No. BK20180915), the Jiangsu Agriculture Science and Technology Innovation Fund (No. CX(18)2012), the Fishery Science and Technology Innovation Projects of Jiangsu Province (No. D2017-3), the “Blue Project” of Yangzhou University and the Projects of Shuichan Sanxin of Jiangsu Province (No. Y2016-33, D2017-3)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Liu, X., Gao, X., Chen, N. et al. Transcriptional responses to starvation of pathogenic Vibrio harveyi strain DY1. J. Ocean. Limnol. 38, 579–587 (2020). https://doi.org/10.1007/s00343-019-8350-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00343-019-8350-3

Keyword

Search

Navigation