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Chapter 13 : Species

Authors: Daniela Ceccarelli1, Carmen Amaro2, Jesús L. Romalde3, Elisabetta Suffredini4, Luigi Vezzulli5
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Affiliations: 1: Department of Bacteriology and Epidemiology, Wageningen Bioveterinary Research, Lelystad, The Netherlands; 2: ERI BioTecMed, Department of Microbiology and Ecology, University of Valencia, Faculty of Biology, Campus of Burjassot, Valencia, Spain; 3: Department of Microbiology and Parasitology, Universidade de Santiago de Compostela, Santiago de Compostela, Spain; 4: Department of Food Safety, Nutrition and Veterinary Public Health, Istituto Superiore di Sanitá, Rome, Italy; 5: Department of Earth, Environmental and Life Science, University of Genova, Genova, Italy
Content Type: Reference
Publication Year: 2019

Category: Food Microbiology

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Abstract:

The genus contains 130 confirmed species, of which a dozen have been demonstrated to cause infections in humans. As vibrios are natural inhabitants of aquatic environments, infections are usually associated with wound exposure to seawater or consumption of raw seafood. As estimated by the Centers for Disease Control and Prevention, vibriosis causes approximately 80,000 illnesses and 100 deaths in the United States every year, mostly during the summer months, when water temperatures are warmer, and in contrast to infections caused by other major foodborne pathogens, the number of infections is steadily increasing. Several reports have recently indicated that human illnesses are increasing worldwide, as well as the species responsible for these infections. Besides “the big four” (, , , and ), additional species [, , () , , , and ] have recently been associated with food consumption. These 10 species are the subject of this chapter.

Citation: Ceccarelli D, Amaro C, Romalde J, Suffredini E, Vezzulli L. 2019. Species, p 347-388. In Doyle M, Diez-Gonzalez F, Hill C (ed), Food Microbiology: Fundamentals and Frontiers, 5th Edition. ASM Press, Washington, DC. doi: 10.1128/9781555819972.ch13
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Vibrio Species
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Citation: Ceccarelli D, Amaro C, Romalde J, Suffredini E, Vezzulli L. 2019. Species, p 347-388. In Doyle M, Diez-Gonzalez F, Hill C (ed), Food Microbiology: Fundamentals and Frontiers, 5th Edition. ASM Press, Washington, DC. doi: 10.1128/9781555819972.ch13
/content/10.1128/9781555819972.ch13.ch13fig1
Figure 13.1
Scheme for the isolation and identification of spp. from seafood, water, and sediment samples; adapted from FDA protocols ( ). Once the bacterium has been isolated and identified, the pure culture should be maintained at –80°C in LB or tryptic soy broth supplemented with 15 to 20% glycerol. MPN, most probable number; APW 1-2%, alkaline peptone water containing 1 to 2% NaCl; TTGA, taurocholate-tellurite-gelatin agar; VVM, medium. For more details and species-specific PCR, see “Isolation” and sections on individual species in the text.
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Figure 13.1

Scheme for the isolation and identification of spp. from seafood, water, and sediment samples; adapted from FDA protocols ( ). Once the bacterium has been isolated and identified, the pure culture should be maintained at –80°C in LB or tryptic soy broth supplemented with 15 to 20% glycerol. MPN, most probable number; APW 1-2%, alkaline peptone water containing 1 to 2% NaCl; TTGA, taurocholate-tellurite-gelatin agar; VVM, medium. For more details and species-specific PCR, see “Isolation” and sections on individual species in the text.

Citation: Ceccarelli D, Amaro C, Romalde J, Suffredini E, Vezzulli L. 2019. Species, p 347-388. In Doyle M, Diez-Gonzalez F, Hill C (ed), Food Microbiology: Fundamentals and Frontiers, 5th Edition. ASM Press, Washington, DC. doi: 10.1128/9781555819972.ch13
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Figure 13.2
Cholera toxin mechanism. After ingestion, cells colonize the intestinal lumen (step 1), where they start secreting cholera toxin (Ctx), which is composed of two toxic subunits (A1 and A2) and five binding (B) units (step 2). The complete toxin binds to the GM1 ganglioside receptors on the cell membrane (step 3) via the binding subunits. NanH facilitates Ctx binding to host cells by converting cell surface gangliosides to GM1 gangliosides (step 4). This interaction triggers the internalization of the toxin via an endosome in the cell (step 5). Once in the cell, the reduction of the A and B subunits occurs in the endoplasmic reticulum, leaving the B subunits in the endoplasmic reticulum. The active A1 subunit is then released into the cytosol, where it catalyzes the ADP-ribosylation of the G regulatory protein, which regulates the activation of the adenylate cyclase (AC) system (step 6). The constant active state of G provokes a persistent activation of AC, which results in accumulation of cyclic AMP (cAMP) along the cell membrane. The cAMP causes the active secretion (step 7) of sodium (Na), chloride (Cl), potassium (K), bicarbonate (HCO), and water (HO) into the intestinal lumen, which is clinically associated with profuse diarrhea and dehydration. The accessory toxin Zot (step 8) induces modifications of cytoskeletal organization that lead to the opening of tight junctions, increasing the permeability of the small intestine. Data are from reference .
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Figure 13.2

Cholera toxin mechanism. After ingestion, cells colonize the intestinal lumen (step 1), where they start secreting cholera toxin (Ctx), which is composed of two toxic subunits (A1 and A2) and five binding (B) units (step 2). The complete toxin binds to the GM1 ganglioside receptors on the cell membrane (step 3) via the binding subunits. NanH facilitates Ctx binding to host cells by converting cell surface gangliosides to GM1 gangliosides (step 4). This interaction triggers the internalization of the toxin via an endosome in the cell (step 5). Once in the cell, the reduction of the A and B subunits occurs in the endoplasmic reticulum, leaving the B subunits in the endoplasmic reticulum. The active A1 subunit is then released into the cytosol, where it catalyzes the ADP-ribosylation of the G regulatory protein, which regulates the activation of the adenylate cyclase (AC) system (step 6). The constant active state of G provokes a persistent activation of AC, which results in accumulation of cyclic AMP (cAMP) along the cell membrane. The cAMP causes the active secretion (step 7) of sodium (Na), chloride (Cl), potassium (K), bicarbonate (HCO), and water (HO) into the intestinal lumen, which is clinically associated with profuse diarrhea and dehydration. The accessory toxin Zot (step 8) induces modifications of cytoskeletal organization that lead to the opening of tight junctions, increasing the permeability of the small intestine. Data are from reference .

Citation: Ceccarelli D, Amaro C, Romalde J, Suffredini E, Vezzulli L. 2019. Species, p 347-388. In Doyle M, Diez-Gonzalez F, Hill C (ed), Food Microbiology: Fundamentals and Frontiers, 5th Edition. ASM Press, Washington, DC. doi: 10.1128/9781555819972.ch13
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Figure 13.3
Life cycle of . (Step 1) Resuscitation. VBNC bacteria resuscitate when temperature increases to more than 10°C. (Step 2) Uptake by filter feeders, ingestion by humans, and infection. Bacteria with or without flagella can be taken up by filter feeders, such as oysters, which, in turn, can be ingested by humans. (Step 3) Chemotaxis through blood. Flagellated bacteria can be attracted by blood and colonize wounds on animal and human surfaces. (Step 4) Animal septicemia: fish vibriosis. In the case of animals, only bacteria possessing the virulence plasmid pVvBt2 colonize and invade blood, causing fish vibriosis. (Step 5) Human infection by fish and seafood handling. (Step 6) Human septicemia. In the case of humans, regardless of the route of infection (ingestion or contact), bacteria have success in invasion and in causing septicemia, mainly in iron-overloaded patients. (Step 7) Humans are the end hosts for infection. (Step 8) Dispersion of cells from infected aquatic animals into the water. (Step 9) Bacteria can form biofilms on mucosal and inert surfaces, from which they can be dispersed again into the water. (Step 10) Induction of the VBNC state. When the temperature drops below 10°C, bacteria enter the VBNC state, closing the cycle. Adapted from reference .
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Figure 13.3

Life cycle of . (Step 1) Resuscitation. VBNC bacteria resuscitate when temperature increases to more than 10°C. (Step 2) Uptake by filter feeders, ingestion by humans, and infection. Bacteria with or without flagella can be taken up by filter feeders, such as oysters, which, in turn, can be ingested by humans. (Step 3) Chemotaxis through blood. Flagellated bacteria can be attracted by blood and colonize wounds on animal and human surfaces. (Step 4) Animal septicemia: fish vibriosis. In the case of animals, only bacteria possessing the virulence plasmid pVvBt2 colonize and invade blood, causing fish vibriosis. (Step 5) Human infection by fish and seafood handling. (Step 6) Human septicemia. In the case of humans, regardless of the route of infection (ingestion or contact), bacteria have success in invasion and in causing septicemia, mainly in iron-overloaded patients. (Step 7) Humans are the end hosts for infection. (Step 8) Dispersion of cells from infected aquatic animals into the water. (Step 9) Bacteria can form biofilms on mucosal and inert surfaces, from which they can be dispersed again into the water. (Step 10) Induction of the VBNC state. When the temperature drops below 10°C, bacteria enter the VBNC state, closing the cycle. Adapted from reference .

Citation: Ceccarelli D, Amaro C, Romalde J, Suffredini E, Vezzulli L. 2019. Species, p 347-388. In Doyle M, Diez-Gonzalez F, Hill C (ed), Food Microbiology: Fundamentals and Frontiers, 5th Edition. ASM Press, Washington, DC. doi: 10.1128/9781555819972.ch13
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Figure 13.4
Clinical signs of human sepsis caused by . The photo shows typical clinical signs of primary and secondary sepsis caused by : swelling, erythema, development of vesicles or bullae, and tissue necrosis. Picture courtesy of Ching-Chuan Liu, Department of Pediatrics, National Cheng Kung University Hospital, College of Medicine, National Cheng Kung University, Tainan City, Taiwan.
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Figure 13.4

Clinical signs of human sepsis caused by . The photo shows typical clinical signs of primary and secondary sepsis caused by : swelling, erythema, development of vesicles or bullae, and tissue necrosis. Picture courtesy of Ching-Chuan Liu, Department of Pediatrics, National Cheng Kung University Hospital, College of Medicine, National Cheng Kung University, Tainan City, Taiwan.

Citation: Ceccarelli D, Amaro C, Romalde J, Suffredini E, Vezzulli L. 2019. Species, p 347-388. In Doyle M, Diez-Gonzalez F, Hill C (ed), Food Microbiology: Fundamentals and Frontiers, 5th Edition. ASM Press, Washington, DC. doi: 10.1128/9781555819972.ch13
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Figure 13.5
Steps in colonization, invasion, and sepsis caused by and role of selected genes. (A) Colonization. cells arrive at the intestine; some are eliminated, but others are attracted by mucin and bind to it by Gbp (step 1). Mucin-coated cells bind to mucin receptors on epithelial cells (step 2). Attached cells produce VvpE, VvhA, and RtxA1, whose joint activity results in increased permeability and tight-junction disruption (step 3). Cells pass through the epithelium and continue producing Vvp, VvhA, and RtxA1, which cause cell death by different mechanisms (step 4). Attacked cells secrete cytokines (CK) and chemokines (CC), which triggers local inflammation (step 5). VvpE inhibits mucin secretion (step 6), which in turn facilitates vibrio adhesion, in this case probably by the interaction between pili/flagellin and Toll-like receptors (TLR) (step 7). Established bacteria will multiply on the epithelium. (B) Invasion and sepsis. Inflammation alters endothelial cells, enabling bacteria to cross the endothelial barrier (step 8). Bacteria multiply in blood thanks to the combination of a series of protective mechanisms in which capsule, LPS, KtrA, and RtxA1 are involved (step 9). Bacteria interact with different immune cells and, finally, cause sepsis and death, probably by inducing a cytokine storm (step 10). The figure is not to scale. PRRs, pattern recognition receptors. Adapted from reference 204.
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Figure 13.5

Steps in colonization, invasion, and sepsis caused by and role of selected genes. (A) Colonization. cells arrive at the intestine; some are eliminated, but others are attracted by mucin and bind to it by Gbp (step 1). Mucin-coated cells bind to mucin receptors on epithelial cells (step 2). Attached cells produce VvpE, VvhA, and RtxA1, whose joint activity results in increased permeability and tight-junction disruption (step 3). Cells pass through the epithelium and continue producing Vvp, VvhA, and RtxA1, which cause cell death by different mechanisms (step 4). Attacked cells secrete cytokines (CK) and chemokines (CC), which triggers local inflammation (step 5). VvpE inhibits mucin secretion (step 6), which in turn facilitates vibrio adhesion, in this case probably by the interaction between pili/flagellin and Toll-like receptors (TLR) (step 7). Established bacteria will multiply on the epithelium. (B) Invasion and sepsis. Inflammation alters endothelial cells, enabling bacteria to cross the endothelial barrier (step 8). Bacteria multiply in blood thanks to the combination of a series of protective mechanisms in which capsule, LPS, KtrA, and RtxA1 are involved (step 9). Bacteria interact with different immune cells and, finally, cause sepsis and death, probably by inducing a cytokine storm (step 10). The figure is not to scale. PRRs, pattern recognition receptors. Adapted from reference 204.

Citation: Ceccarelli D, Amaro C, Romalde J, Suffredini E, Vezzulli L. 2019. Species, p 347-388. In Doyle M, Diez-Gonzalez F, Hill C (ed), Food Microbiology: Fundamentals and Frontiers, 5th Edition. ASM Press, Washington, DC. doi: 10.1128/9781555819972.ch13
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Figure 13.6
Structure (A) and mode of action at the cellular level (B) of MARTX type I of (also called RtxA11). (A) The scheme shows the conserved external modules and the internal module, containing the five effector domains. (B) The toxin is secreted and the external module is associated with the target cell membrane by forming a pore that allows the central module to be exposed to the cytosol. The cysteine protease domain (CPD) catalyzes the release of the rest of internal domains after being activated by binding inositol hexakisphosphate. The domain with unknown function (DUF1) probably binds prohibitin-1, promoting the translocation of the toxin into the cell. The Rho GTPase inhibitor (RID) activates actin depolymerization, altering the cell cytoskeleton. The alpha/beta hydrolase domain (ABH) binds inositol 3-phosphate and inhibits autophagy and endosomal trafficking. The MCF (makes caterpillars floppy)-like domain induces depolarization of the mitochondrial membrane potential, which causes activation of cell death. The Ras/Rap1 specific endopeptidase domain (RRSP) suppresses the ERK–mitogen-activated protein kinase pathway by proteolytically processing Ras and Rap1 GTPases, preventing Ras from activating ERK, and then inhibiting cell proliferation. For more details on MARTX action at the cellular level, see reference 198. The figure is not to scale.
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Figure 13.6

Structure (A) and mode of action at the cellular level (B) of MARTX type I of (also called RtxA11). (A) The scheme shows the conserved external modules and the internal module, containing the five effector domains. (B) The toxin is secreted and the external module is associated with the target cell membrane by forming a pore that allows the central module to be exposed to the cytosol. The cysteine protease domain (CPD) catalyzes the release of the rest of internal domains after being activated by binding inositol hexakisphosphate. The domain with unknown function (DUF1) probably binds prohibitin-1, promoting the translocation of the toxin into the cell. The Rho GTPase inhibitor (RID) activates actin depolymerization, altering the cell cytoskeleton. The alpha/beta hydrolase domain (ABH) binds inositol 3-phosphate and inhibits autophagy and endosomal trafficking. The MCF (makes caterpillars floppy)-like domain induces depolarization of the mitochondrial membrane potential, which causes activation of cell death. The Ras/Rap1 specific endopeptidase domain (RRSP) suppresses the ERK–mitogen-activated protein kinase pathway by proteolytically processing Ras and Rap1 GTPases, preventing Ras from activating ERK, and then inhibiting cell proliferation. For more details on MARTX action at the cellular level, see reference 198. The figure is not to scale.

Citation: Ceccarelli D, Amaro C, Romalde J, Suffredini E, Vezzulli L. 2019. Species, p 347-388. In Doyle M, Diez-Gonzalez F, Hill C (ed), Food Microbiology: Fundamentals and Frontiers, 5th Edition. ASM Press, Washington, DC. doi: 10.1128/9781555819972.ch13
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References

/content/book/10.1128/9781555819972.ch13
1. Baker-Austin C, Trinanes J, Gonzalez-Escalona N, Martinez-Urtaza J . 2017. Non-cholera vibrios: the microbial barometer of climate change. Trends Microbiol 25 : 76– 84.[CrossRef][PubMed]
2. Centers for Disease Control and Prevention . 2016. National enteric disease surveillance: cholera and other Vibrio illness surveillance annual summary, 2014. Centers for Disease Control and Prevention, Atlanta, GA.
3. Conner JG, Teschler JK, Jones CJ, Yildiz FH . 2016. Staying alive: Vibrio cholerae's cycle of environmental survival, transmission, and dissemination. Microbiol Spectr 4 : VMBF-0015-2015.[PubMed]
4. Vezzulli L, Colwell RR, Pruzzo C . 2013. Ocean warming and spread of pathogenic vibrios in the aquatic environment. Microb Ecol 65 : 817– 825.[CrossRef][PubMed]
5. Baker-Austin C, Trinanes JA, Taylor NGH, Hartnell R, Siitonen A, Martinez-Urtaza J . 2013. Emerging Vibrio risk at high latitudes in response to ocean warming. Nat Clim Chang 3 : 73– 77. CORRIGENDUM Nat Clim Chang 6 : 802..[CrossRef]
6. Reen FJ, Almagro-Moreno S, Ussery D, Boyd EF . 2006. The genomic code: inferring Vibrionaceae niche specialization. Nat Rev Microbiol 4 : 697– 704.[CrossRef][PubMed]
7. Iwamoto M, Ayers T, Mahon BE, Swerdlow DL . 2010. Epidemiology of seafood-associated infections in the United States. Clin Microbiol Rev 23 : 399– 411.[CrossRef][PubMed]
8. Newton A, Kendall M, Vugia DJ, Henao OL, Mahon BE . 2012. Increasing rates of vibriosis in the United States, 1996-2010: review of surveillance data from 2 systems. Clin Infect Dis 54( Suppl 5) : S391– S395.[CrossRef][PubMed]
9. Kaysner CA, DePaola A Jr . 2004. Vibrio. In Bacteriological Analytical Manual. U.S. Food and Drug Administration, Rockville, MD.
10. Cerdà-Cuéllar M, Jofre J, Blanch AR . 2000. A selective medium and a specific probe for detection of Vibrio vulnificus. Appl Environ Microbiol 66 : 855– 859.[CrossRef][PubMed]
11. Oliver JD, . 2012. Culture media for the isolation and enumeration of pathogenic Vibrio species in foods and environmental samples, p. 377– 402. In Corry JEL,, Curtis GDW,, Baird RM (ed.), Handbook of Culture Media for Food and Water Microbiology, 3rd ed. Royal Society of Chemistry, Cambridge, United Kingdom.
12. O'Hara CM, Sowers EG, Bopp CA, Duda SB, Strockbine NA . 2003. Accuracy of six commercially available systems for identification of members of the family Vibrionaceae. J Clin Microbiol 41 : 5654– 5659.[CrossRef][PubMed]
13. Abbott SL, Janda JM, Johnson JA, Farmer JJ III, . 2007. Vibrio and related organisms, p. 723–733. In Murray PR, Baron EJ, Jorgensen JH, Landry ML, Pfaller MA (ed), Manual of Clinical Microbiology, 9th ed. ASM Press, Washington, DC.
14. Ramamurthy T, Chowdhury G, Pazhani GP, Shinoda S . 2014. Vibrio fluvialis: an emerging human pathogen. Front Microbiol 5 : 91.[CrossRef][PubMed]
15. Silvester R, Alexander D, Antony AC, Hatha M . 2017. GroEL PCR-RFLP—an efficient tool to discriminate closely related pathogenic Vibrio species. Microb Pathog 105 : 196– 200.[CrossRef][PubMed]
16. Senachai P, Chomvarin C, Namwat W, Wongboot W, Wongwajana S, Tangkanakul W . 2013. Application of tetraplex PCR for detection of Vibrio cholerae, V. parahaemolyticus, V. vulnificus and V. mimicus in cockle. Southeast Asian J Trop Med Public Health 44 : 249– 258.[PubMed]
17. Cariani A, Piano A, Consolandi C, Severgnini M, Castiglioni B, Caredda G, Candela M, Serratore P, De Bellis G, Tinti F . 2012. Detection and characterization of pathogenic vibrios in shellfish by a ligation detection reaction-universal array approach. Int J Food Microbiol 153 : 474– 482.[CrossRef][PubMed]
18. Banerjee SK, Farber JM . 2017. Detection, enumeration, and isolation of Vibrio parahaemolyticus and V. vulnificus from seafood: development of a multidisciplinary protocol. J AOAC Int 100 : 445– 453.[CrossRef][PubMed]
19. Griffitt KJ, Grimes DJ . 2013. A novel agar formulation for isolation and direct enumeration of Vibrio vulnificus from oyster tissue. J Microbiol Methods 94 : 98– 102.[CrossRef][PubMed]
20. Suffredini E, Cozzi L, Ciccaglioni G, Croci L . 2014. Development of a colony hybridization method for the enumeration of total and potentially enteropathogenic Vibrio parahaemolyticus in shellfish. Int J Food Microbiol 186 : 22– 31.[CrossRef][PubMed]
21. Ronholm J, Lau F, Banerjee SK . 2016. Emerging seafood preservation techniques to extend freshness and minimize Vibrio contamination. Front Microbiol 7 : 350.[CrossRef][PubMed]
22. Larsen AM, Rikard FS, Walton WC, Arias CR . 2015. Temperature effect on high salinity depuration of Vibrio vulnificus and V. parahaemolyticus from the Eastern oyster ( Crassostrea virginica). Int J Food Microbiol 192 : 66– 71.[CrossRef][PubMed]
23. Larsen AM, Rikard FS, Walton WC, Arias CR . 2013. Effective reduction of Vibrio vulnificus in the Eastern oyster ( Crassostrea virginica) using high salinity depuration. Food Microbiol 34 : 118– 122.[CrossRef][PubMed]
24. Parveen S, Jahncke M, Elmahdi S, Crocker H, Bowers J, White C, Gray S, Morris AC, Brohawn K . 2017. High salinity relaying to reduce Vibrio parahaemolyticus and Vibrio vulnificus in Chesapeake Bay oysters ( Crassostrea virginica). J Food Sci 82 : 484– 491.[CrossRef][PubMed]
25. Baker GL . 2016. Food safety impacts from post-harvest processing procedures of molluscan shellfish. Foods 5 : 29.[CrossRef][PubMed]
26. U.S. Food and Drug Administration . 2017. National Shellfish Sanitation Program (NSSP) guide for the control of molluscan shellfish, 2015 revision (updated February 2017). U.S. Food and Drug Administration, Washington, DC.
27. Asakura H, Ishiwa A, Arakawa E, Makino S, Okada Y, Yamamoto S, Igimi S . 2007. Gene expression profile of Vibrio cholerae in the cold stress-induced viable but non-culturable state. Environ Microbiol 9 : 869– 879.[CrossRef][PubMed]
28. Urmersbach S, Aho T, Alter T, Hassan SS, Autio R, Huehn S . 2015. Changes in global gene expression of Vibrio parahaemolyticus induced by cold- and heat-stress. BMC Microbiol 15 : 229.[CrossRef][PubMed]
29. Choi S, Jang KK, Choi S, Yun HJ, Kang D-H . 2012. Identification of the Vibrio vulnificus htpG gene and its influence on cold shock recovery. J Microbiol 50 : 707– 711. ERRATUM J Microbiol 53 : 739..[CrossRef][PubMed]
30. Li Z, Jia J, Cao J, Chen J, Xu Q, Jiang Y . 2013. Identification of Vibrio metschnikovii from Homarus americanus and its changes in membrane fatty acid composition in response to low temperature. Wei Sheng Wu Xue Bao 53 : 628– 634. [In Chinese.][PubMed]
31. Wong H-C, Chen L-L, Yu C-M . 1994. Survival of psychrotrophic Vibrio mimicus, Vibrio fluvialis and Vibrio parahaemolyticus in culture broth at low temperatures. J Food Prot 57 : 607– 610.[CrossRef].
32. Food and Drug Administration, HHS . 2005. Irradiation in the production, processing, and handling of food. Final rule. Fed Regist 70 : 48057– 48073.[PubMed]
33. Mahmoud BS . 2009. Effect of X-ray treatments on inoculated Escherichia coli O157: H7, Salmonella enterica, Shigella flexneri and Vibrio parahaemolyticus in ready-to-eat shrimp. Food Microbiol 26 : 860– 864.[CrossRef][PubMed]
34. Jakabi M, Gelli DS, Torre JC, Rodas MA, Franco BD, Destro MT, Landgraf M . 2003. Inactivation by ionizing radiation of Salmonella enteritidis, Salmonella infantis, and Vibrio parahaemolyticus in oysters ( Crassostrea brasiliana). J Food Prot 66 : 1025– 1029.[CrossRef][PubMed]
35. Mahmoud BS . 2009. Reduction of Vibrio vulnificus in pure culture, half shell and whole shell oysters ( Crassostrea virginica) by X-ray. Int J Food Microbiol 130 : 135– 139.[CrossRef][PubMed]
36. Considine KM, Kelly AL, Fitzgerald GF, Hill C, Sleator RD . 2008. High-pressure processing—effects on microbial food safety and food quality. FEMS Microbiol Lett 281 : 1– 9.[CrossRef][PubMed]
37. Ye M, Huang Y, Gurtler JB, Niemira BA, Sites JE, Chen H . 2013. Effects of pre- or post-processing storage conditions on high-hydrostatic pressure inactivation of Vibrio parahaemolyticus and V. vulnificus in oysters. Int J Food Microbiol 163 : 146– 152.[CrossRef][PubMed]
38. Phuvasate S, Su YC . 2015. Efficacy of low-temperature high hydrostatic pressure processing in inactivating Vibrio parahaemolyticus in culture suspension and oyster homogenate. Int J Food Microbiol 196 : 11– 15.[CrossRef][PubMed]
39. Jun JW, Kim HJ, Yun SK, Chai JY, Park SC . 2014. Eating oysters without risk of vibriosis: application of a bacteriophage against Vibrio parahaemolyticus in oysters. Int J Food Microbiol 188 : 31– 35.[CrossRef][PubMed]
40. Teplitski M, Wright AC, Lorca G . 2009. Biological approaches for controlling shellfish-associated pathogens. Curr Opin Biotechnol 20 : 185– 190.[CrossRef][PubMed]
41. Chowdhury FR, Nur Z, Hassan N, von Seidlein L, Dunachie S . 2017. Pandemics, pathogenicity and changing molecular epidemiology of cholera in the era of global warming. Ann Clin Microbiol Antimicrob 16 : 10.[CrossRef][PubMed]
42. Kaper JB, Morris JG Jr, Levine MM . 1995. Cholera. Clin Microbiol Rev 8 : 48– 86.[PubMed]
43. Safa A, Nair GB, Kong RYC . 2010. Evolution of new variants of Vibrio cholerae O1. Trends Microbiol 18 : 46– 54.[CrossRef][PubMed]
44. Chin C-S, Sorenson J, Harris JB, Robins WP, Charles RC, Jean-Charles RR, Bullard J, Webster DR, Kasarskis A, Peluso P, Paxinos EE, Yamaichi Y, Calderwood SB, Mekalanos JJ, Schadt EE, Waldor MK . 2011. The origin of the Haitian cholera outbreak strain. N Engl J Med 364 : 33– 42.[CrossRef][PubMed]
45. Goel AK, Jain M, Kumar P, Bhadauria S, Kmboj DV, Singh L . 2008. A new variant of Vibrio cholerae O1 El Tor causing cholera in India. J Infect 57 : 280– 281.[CrossRef][PubMed]
46. Cho YJ, Yi H, Lee JH, Kim DW, Chun J . 2010. Genomic evolution of Vibrio cholerae. Curr Opin Microbiol 13 : 646– 651.[CrossRef][PubMed]
47. Grim CJ, Hasan NA, Taviani E, Haley B, Chun J, Brettin TS, Bruce DC, Detter JC, Han CS, Chertkov O, Challacombe J, Huq A, Nair GB, Colwell RR . 2010. Genome sequence of hybrid Vibrio cholerae O1 MJ-1236, B-33, and CIRS101 and comparative genomics with V. cholerae. J Bacteriol 192 : 3524– 3533.[CrossRef][PubMed]
48. Raychoudhuri A, Mukhopadhyay AK, Ramamurthy T, Nandy RK, Takeda Y, Nair GB . 2008. Biotyping of Vibrio cholerae O1: time to redefine the scheme. Indian J Med Res 128 : 695– 698.[PubMed]
49. Albert MJ . 1994. Vibrio cholerae O139 Bengal. J Clin Microbiol 32 : 2345– 2349.[PubMed]
50. Dutta D, Chowdhury G, Pazhani GP, Guin S, Dutta S, Ghosh S, Rajendran K, Nandy RK, Mukhopadhyay AK, Bhattacharya MK, Mitra U, Takeda Y, Nair GB, Ramamurthy T . 2013. Vibrio cholerae non-O1, non-O139 serogroups and cholera-like diarrhea, Kolkata, India. Emerg Infect Dis 19 : 464– 467.[CrossRef][PubMed]
51. Albert MJ, Nair GB . 2005. Vibrio cholerae O139 Bengal—10 years on. Rev Med Microbiol 16 : 135– 143.[CrossRef].
52. Hirk S, Huhulescu S, Allerberger F, Lepuschitz S, Rehak S, Weil S, Gschwandtner E, Hermann M, Neuhold S, Zoufaly A, Indra A . 2016. Necrotizing fasciitis due to Vibrio cholerae non-O1/non-O139 after exposure to Austrian bathing sites. Wien Klin Wochenschr 128 : 141– 145.[CrossRef][PubMed]
53. Khan S, Kumar A, Meparambu D, Thomas S, Harichandran D, Karim S . 2013. Fatal non-O1, non-O139 Vibrio cholerae septicaemia in a patient with chronic liver disease. J Med Microbiol 62 : 917– 921.[CrossRef][PubMed]
54. Dalsgaard A, Serichantalergs O, Forslund A, Lin W, Mekalanos J, Mintz E, Shimada T, Wells JG . 2001. Clinical and environmental isolates of Vibrio cholerae serogroup O141 carry the CTX phage and the genes encoding the toxin-coregulated pili. J Clin Microbiol 39 : 4086– 4092.[CrossRef][PubMed]
55. Hasan NA, Choi SY, Eppinger M, Clark PW, Chen A, Alam M, Haley BJ, Taviani E, Hine E, Su Q, Tallon LJ, Prosper JB, Furth K, Hoq MM, Li H, Fraser-Liggett CM, Cravioto A, Huq A, Ravel J, Cebula TA, Colwell RR . 2012. Genomic diversity of 2010 Haitian cholera outbreak strains. Proc Natl Acad Sci USA 109 : E2010– E2017.[CrossRef][PubMed]
56. Le Roux F, Wegner KM, Baker-Austin C, Vezzulli L, Osorio CR, Amaro C, Ritchie JM, Defoirdt T, Destoumieux-Garzón D, Blokesch M, Mazel D, Jacq A, Cava F, Gram L, Wendling CC, Strauch E, Kirschner A, Huehn S . 2015. The emergence of Vibrio pathogens in Europe: ecology, evolution, and pathogenesis (Paris, 11-12th March 2015). Front Microbiol 6 : 830.[PubMed]
57. Lyon WJ . 2001. TaqMan PCR for detection of Vibrio cholerae O1, O139, non-O1, and non-O139 in pure cultures, raw oysters, and synthetic seawater. Appl Environ Microbiol 67 : 4685– 4693.[CrossRef][PubMed]
58. Vezzulli L, Stauder M, Grande C, Pezzati E, Verheye HM, Owens NJP, Pruzzo C . 2015. gbpA as a novel qPCR target for the species-specific detection of Vibrio cholerae O1, O139, non-O1/non-O139 in environmental, stool, and historical continuous plankton recorder samples. PLoS One 10 : e0123983.[CrossRef][PubMed]
59. Kumar P, Peter WA, Thomas S . 2010. Rapid detection of virulence-associated genes in environmental strains of Vibrio cholerae by multiplex PCR. Curr Microbiol 60 : 199– 202.[CrossRef][PubMed]
60. Kotetishvili M, Stine OC, Chen Y, Kreger A, Sulakvelidze A, Sozhamannan S, Morris JG Jr . 2003. Multilocus sequence typing has better discriminatory ability for typing Vibrio cholerae than does pulsed-field gel electrophoresis and provides a measure of phylogenetic relatedness. J Clin Microbiol 41 : 2191– 2196.[CrossRef][PubMed]
61. Vora GJ, Meador CE, Bird MM, Bopp CA, Andreadis JD, Stenger DA . 2005. Microarray-based detection of genetic heterogeneity, antimicrobial resistance, and the viable but nonculturable state in human pathogenic Vibrio spp. Proc Natl Acad Sci USA 102 : 19109– 19114.[CrossRef][PubMed]
62. Schadt EE, Linderman MD, Sorenson J, Lee L, Nolan GP . 2010. Computational solutions to large-scale data management and analysis. Nat Rev Genet 11 : 647– 657.[CrossRef][PubMed]
63. Vezzulli L, Grande C, Tassistro G, Brettar I, Höfle MG, Pereira RP, Mushi D, Pallavicini A, Vassallo P, Pruzzo C . 2017. Whole-genome enrichment provides deep insights into Vibrio cholerae metagenome from an African river. Microb Ecol 73 : 734– 738.[CrossRef][PubMed]
64. Sack DA, Sack RB, Nair GB, Siddique AK . 2004. Cholera. Lancet 363 : 223– 233.[CrossRef][PubMed]
65. Suzita R, Abdulamir AS, Bakar FA, Son R . 2009. A mini review: cholera outbreak via shellfish. Am J Infect Dis 5 : 40– 47.[CrossRef].
66. Mintz ED, Popovic T, Blake PA, . 1994. Transmission of Vibrio cholerae O1, p 345– 356. In Wachsmuth IK, Blake PA, Olsvik O (ed), Vibrio cholerae and Cholera: Molecular to Global Perspectives. ASM Press, Washington, DC.[CrossRef]
67. Pruzzo C, Vezzulli L, Colwell RR . 2008. Global impact of Vibrio cholerae interactions with chitin. Environ Microbiol 10 : 1400– 1410.[CrossRef][PubMed]
68. Tobin-D'Angelo M, Smith AR, Bulens SN, Thomas S, Hodel M, Izumiya H, Arakawa E, Morita M, Watanabe H, Marin C, Parsons MB, Greene K, Cooper K, Haydel D, Bopp C, Yu P, Mintz E . 2008. Severe diarrhea caused by cholera toxin-producing vibrio cholerae serogroup O75 infections acquired in the southeastern United States. Clin Infect Dis 47 : 1035– 1040.[CrossRef][PubMed]
69. Morris JG Jr . 1990. Non-O group 1 Vibrio cholerae: a look at the epidemiology of an occasional pathogen. Epidemiol Rev 12 : 179– 191.[CrossRef][PubMed]
70. Vezzulli L, Pruzzo C, Huq A, Colwell RR . 2010. Environmental reservoirs of Vibrio cholerae and their role in cholera. Environ Microbiol Rep 2 : 27– 33.[CrossRef][PubMed]
71. Colwell RR . 1996. Global climate and infectious disease: the cholera paradigm. Science 274 : 2025– 2031.[CrossRef][PubMed]
72. Oliver JD, . 2005. Viable but nonculturable bacteria in food environments, p 99– 112. In Fratamico PM, Bhunia AK, Smith JL (ed), Food-Borne Pathogens: Microbiology and Molecular Biology. Caister Academic Press, Norfolk, United Kingdom.
73. Colwell RR, Huq A, Islam MS, Aziz KMA, Yunus M, Khan NH, Mahmud A, Sack RB, Nair GB, Chakraborty J, Sack DA, Russek-Cohen E . 2003. Reduction of cholera in Bangladeshi villages by simple filtration. Proc Natl Acad Sci USA 100 : 1051– 1055.[CrossRef][PubMed]
74. Watnick PI, Kolter R . 1999. Steps in the development of a Vibrio cholerae El Tor biofilm. Mol Microbiol 34 : 586– 595.[CrossRef][PubMed]
75. Nelson EJ, Harris JB, Morris JG Jr, Calderwood SB, Camilli A . 2009. Cholera transmission: the host, pathogen and bacteriophage dynamic. Nat Rev Microbiol 7 : 693– 702.[CrossRef][PubMed]
76. Faruque SM, Naser IB, Islam MJ, Faruque AS, Ghosh AN, Nair GB, Sack DA, Mekalanos JJ . 2005. Seasonal epidemics of cholera inversely correlate with the prevalence of environmental cholera phages. Proc Natl Acad Sci USA 102 : 1702– 1707.[CrossRef][PubMed]
77. Levine MM, Black RE, Clements ML, Nalin DR, Cisneros L, , Finkelstein RA. 1981. Volunteer studies in development of vaccines against cholera and enterotoxigenic Escherichia coli: a review, p. 443– 459. In Holme T,, Holmgren J,, Merson MH,, Mollby R (ed.), Acute Enteric Infections in Children: New Prospects for Treatment and Prevention. Elsevier/North-Holland Biomedical Press, Amsterdam, The Netherlands.
78. Almagro-Moreno S, Pruss K, Taylor RK . 2015. Intestinal colonization dynamics of Vibrio cholerae. PLoS Pathog 11 : e1004787.[CrossRef][PubMed]
79. McLeod SM, Kimsey HH, Davis BM, Waldor MK . 2005. CTXphi and Vibrio cholerae: exploring a newly recognized type of phage-host cell relationship. Mol Microbiol 57 : 347– 356.[CrossRef][PubMed]
80. De Haan L, Hirst TR . 2004. Cholera toxin: a paradigm for multi-functional engagement of cellular mechanisms (review). Mol Membr Biol 21 : 77– 92.[CrossRef][PubMed]
81. Sánchez J, Holmgren J . 2008. Cholera toxin structure, gene regulation and pathophysiological and immunological aspects. Cell Mol Life Sci 65 : 1347– 1360.[CrossRef][PubMed]
82. Fasano A, Baudry B, Pumplin DW, Wasserman SS, Tall BD, Ketley JM, Kaper JB . 1991. Vibrio cholerae produces a second enterotoxin, which affects intestinal tight junctions. Proc Natl Acad Sci USA 88 : 5242– 5246.[CrossRef][PubMed]
83. Trucksis M, Galen JE, Michalski J, Fasano A, Kaper JB . 1993. Accessory cholera enterotoxin ( Ace), the third toxin of a Vibrio cholerae virulence cassette. Proc Natl Acad Sci USA 90 : 5267– 5271.[CrossRef][PubMed]
84. Wu Z, Nybom P, Magnusson KE . 2000. Distinct effects of Vibrio cholerae haemagglutinin/protease on the structure and localization of the tight junction-associated proteins occludin and ZO-1. Cell Microbiol 2 : 11– 17.[CrossRef][PubMed]
85. Debellis L, Diana A, Arcidiacono D, Fiorotto R, Portincasa P, Altomare DF, Spirlì C, de Bernard M . 2009. The Vibrio cholerae cytolysin promotes chloride secretion from intact human intestinal mucosa. PLoS One 4 : e5074.[CrossRef][PubMed]
86. Lin W, Fullner KJ, Clayton R, Sexton JA, Rogers MB, Calia KE, Calderwood SB, Fraser C, Mekalanos JJ . 1999. Identification of a vibrio cholerae RTX toxin gene cluster that is tightly linked to the cholera toxin prophage. Proc Natl Acad Sci USA 96 : 1071– 1076.[CrossRef][PubMed]
87. Satchell KJF . 2015. Multifunctional-autoprocessing repeats-in-toxin (MARTX) toxins of vibrios. Microbiol Spectr 3 : VE-0002-2014.[CrossRef][PubMed]
88. Morris JG Jr, Takeda T, Tall BD, Losonsky GA, Bhattacharya SK, Forrest BD, Kay BA, Nishibuchi M . 1990. Experimental non-O group 1 Vibrio cholerae gastroenteritis in humans. J Clin Invest 85 : 697– 705.[CrossRef][PubMed]
89. Taylor RK, Miller VL, Furlong DB, Mekalanos JJ . 1987. Use of phoA gene fusions to identify a pilus colonization factor coordinately regulated with cholera toxin. Proc Natl Acad Sci USA 84 : 2833– 2837.[CrossRef][PubMed]
90. Faruque SM, Mekalanos JJ . 2012. Phage-bacterial interactions in the evolution of toxigenic Vibrio cholerae. Virulence 3 : 556– 565.[CrossRef][PubMed]
91. Karaolis DKR, Johnson JA, Bailey CC, Boedeker EC, Kaper JB, Reeves PR . 1998. A Vibrio cholerae pathogenicity island associated with epidemic and pandemic strains. Proc Natl Acad Sci USA 95 : 3134– 3139.[CrossRef][PubMed]
92. Almagro-Moreno S, Boyd EF . 2009. Sialic acid catabolism confers a competitive advantage to pathogenic Vibrio cholerae in the mouse intestine. Infect Immun 77 : 3807– 3816.[CrossRef][PubMed]
93. Shin OS, Tam VC, Suzuki M, Ritchie JM, Bronson RT, Waldor MK, Mekalanos JJ . 2011. Type III secretion is essential for the rapidly fatal diarrheal disease caused by non-O1, non-O139 Vibrio cholerae. mBio 2 : e00106-11.[CrossRef][PubMed]
94. Unterweger D, Kitaoka M, Miyata ST, Bachmann V, Brooks TM, Moloney J, Sosa O, Silva D, Duran-Gonzalez J, Provenzano D, Pukatzki S . 2012. Constitutive type VI secretion system expression gives Vibrio cholerae intra- and interspecific competitive advantages. PLoS One 7 : e48320.[CrossRef][PubMed]
95. Utada AS, Bennett RR, Fong JCN, Gibiansky ML, Yildiz FH, Golestanian R, Wong GCL . 2014. Vibrio cholerae use pili and flagella synergistically to effect motility switching and conditional surface attachment. Nat Commun 5 : 4913.[CrossRef][PubMed]
96. Chiavelli DA, Marsh JW, Taylor RK . 2001. The mannose-sensitive hemagglutinin of Vibrio cholerae promotes adherence to zooplankton. Appl Environ Microbiol 67 : 3220– 3225.[CrossRef][PubMed]
97. Nesper J, Schild S, Lauriano CM, Kraiss A, Klose KE, Reidl J . 2002. Role of Vibrio cholerae O139 surface polysaccharides in intestinal colonization. Infect Immun 70 : 5990– 5996.[CrossRef][PubMed]
98. Butler SM, Camilli A . 2005. Going against the grain: chemotaxis and infection in Vibrio cholerae. Nat Rev Microbiol 3 : 611– 620.[CrossRef][PubMed]
99. Butler SM, Camilli A . 2004. Both chemotaxis and net motility greatly influence the infectivity of Vibrio cholerae. Proc Natl Acad Sci USA 101 : 5018– 5023.[CrossRef][PubMed]
100. Childers BM, Klose KE . 2007. Regulation of virulence in Vibrio cholerae: the ToxR regulon. Future Microbiol 2 : 335– 344.[CrossRef][PubMed]
101. Jung SA, Hawver LA, Ng WL . 2016. Parallel quorum sensing signaling pathways in Vibrio cholerae. Curr Genet 62 : 255– 260.[CrossRef][PubMed]
102. Hammer BK, Bassler BL . 2003. Quorum sensing controls biofilm formation in Vibrio cholerae. Mol Microbiol 50 : 101– 104.[CrossRef][PubMed]
103. Scallan E, Hoekstra RM, Angulo FJ, Tauxe RV, Widdowson MA, Roy SL, Jones JL, Griffin PM . 2011. Foodborne illness acquired in the United States—major pathogens. Emerg Infect Dis 17 : 7– 15.[CrossRef][PubMed]
104. Blanco-Abad V, Ansede-Bermejo J, Rodriguez-Castro A, Martinez-Urtaza J . 2009. Evaluation of different procedures for the optimized detection of Vibrio parahaemolyticus in mussels and environmental samples. Int J Food Microbiol 129 : 229– 236.[CrossRef][PubMed]
105. Odeyemi OA . 2016. Incidence and prevalence of Vibrio parahaemolyticus in seafood: a systematic review and meta-analysis. Springerplus 5 : 464.[CrossRef][PubMed]
106. Hara-Kudo Y, Kumagai S . 2014. Impact of seafood regulations for Vibrio parahaemolyticus infection and verification by analyses of seafood contamination and infection. Epidemiol Infect 142 : 2237– 2247.[CrossRef][PubMed]
107. Wang S, Duan H, Zhang W, Li JW . 2007. Analysis of bacterial foodborne disease outbreaks in China between 1994 and 2005. FEMS Immunol Med Microbiol 51 : 8– 13.[CrossRef][PubMed]
108. Daniels NA, MacKinnon L, Bishop R, Altekruse S, Ray B, Hammond RM, Thompson S, Wilson S, Bean NH, Griffin PM, Slutsker L . 2000. Vibrio parahaemolyticus infections in the United States, 1973-1998. J Infect Dis 181 : 1661– 1666.[CrossRef][PubMed]
109. Centers for Disease Control and Prevention . 1998. Outbreak of Vibrio parahaemolyticus infections associated with eating raw oysters—Pacific Northwest, 1997. MMWR Morb Mortal Wkly Rep 47 : 457– 462.[PubMed]
110. Centers for Disease Control and Prevention . 2006. Vibrio parahaemolyticus infections associated with consumption of raw shellfish—three states, 2006. MMWR Morb Mortal Wkly Rep 55 : 854– 856.[PubMed]
111. Daniels NA, Ray B, Easton A, Marano N, Kahn E, McShan AL II, Del Rosario L, Baldwin T, Kingsley MA, Puhr ND, Wells JG, Angulo FJ . 2000. Emergence of a new Vibrio parahaemolyticus serotype in raw oysters: a prevention quandary. JAMA 284 : 1541– 1545.[CrossRef][PubMed]
112. Centers for Disease Control and Prevention . 1999. Outbreak of Vibrio parahaemolyticus infection associated with eating raw oysters and clams harvested from Long Island Sound—Connecticut, New Jersey, and New York, 1998. MMWR Morb Mortal Wkly Rep 48 : 48– 51.[PubMed]
113. McLaughlin JB, DePaola A, Bopp CA, Martinek KA, Napolilli NP, Allison CG, Murray SL, Thompson EC, Bird MM, Middaugh JP . 2005. Outbreak of Vibrio parahaemolyticus gastroenteritis associated with Alaskan oysters. N Engl J Med 353 : 1463– 1470.[CrossRef][PubMed]
114. Newton AE, Garrett N, Stroika SG, Halpin JL, Turnsek M, Mody RK Centers for Disease Control and Prevention . 2014. Increase in Vibrio parahaemolyticus infections associated with consumption of Atlantic Coast shellfish—2013. MMWR Morb Mortal Wkly Rep 63 : 335– 336.[PubMed]
115. Raszl SM, Froelich BA, Vieira CR, Blackwood AD, Noble RT . 2016. Vibrio parahaemolyticus and Vibrio vulnificus in South America: water, seafood and human infections. J Appl Microbiol 121 : 1201– 1222.[CrossRef][PubMed]
116. Quilici ML, Robert-Pillot A, Picart J, Fournier JM . 2005. Pandemic Vibrio parahaemolyticus O3:K6 spread, France. Emerg Infect Dis 11 : 1148– 1149.[CrossRef][PubMed]
117. Martinez-Urtaza J, Simental L, Velasco D, DePaola A, Ishibashi M, Nakaguchi Y, Nishibuchi M, Carrera-Flores D, Rey-Alvarez C, Pousa A . 2005. Pandemic Vibrio parahaemolyticus O3:K6, Europe. Emerg Infect Dis 11 : 1319– 1320.[CrossRef][PubMed]
118. Ottaviani D, Leoni F, Rocchegiani E, Santarelli S, Canonico C, Masini L, Ditrani V, Carraturo A . 2008. First clinical report of pandemic Vibrio parahaemolyticus O3:K6 infection in Italy. J Clin Microbiol 46 : 2144– 2145.[CrossRef][PubMed]
119. Martinez-Urtaza J, Powell A, Jansa J, Rey JL, Montero OP, Campello MG, López MJ, Pousa A, Valles MJ, Trinanes J, Hervio-Heath D, Keay W, Bayley A, Hartnell R, Baker-Austin C . 2016. Epidemiological investigation of a foodborne outbreak in Spain associated with U.S. West Coast genotypes of Vibrio parahaemolyticus. Springerplus 5 : 87.[CrossRef][PubMed]
120. Raghunath P . 2015. Roles of thermostable direct hemolysin (TDH) and TDH-related hemolysin (TRH) in Vibrio parahaemolyticus. Front Microbiol 5 : 805.[CrossRef][PubMed]
121. Sakazaki R, Tamura K, Kato T, Obara Y, Yamai S . 1968. Studies on the enteropathogenic, facultatively halophilic bacteria, Vibrio parahaemolyticus. 3. Enteropathogenicity. Jpn J Med Sci Biol 21 : 325– 331.[CrossRef][PubMed]
122. Nishibuchi M, Kaper JB . 1995. Thermostable direct hemolysin gene of Vibrio parahaemolyticus: a virulence gene acquired by a marine bacterium. Infect Immun 63 : 2093– 2099.[PubMed]
123. Raimondi F, Kao JP, Fiorentini C, Fabbri A, Donelli G, Gasparini N, Rubino A, Fasano A . 2000. Enterotoxicity and cytotoxicity of Vibrio parahaemolyticus thermostable direct hemolysin in in vitro systems. Infect Immun 68 : 3180– 3185.[CrossRef][PubMed]
124. Nishibuchi M, Kaper JB . 1990. Duplication and variation of the thermostable direct haemolysin ( tdh) gene in Vibrio parahaemolyticus. Mol Microbiol 4 : 87– 99.[CrossRef][PubMed]
125. Baba K, Shirai H, Terai A, Takeda Y, Nishibuchi M . 1991. Analysis of the tdh gene cloned from a tdh gene- and trh gene-positive strain of Vibrio parahaemolyticus. Microbiol Immunol 35 : 253– 258.[CrossRef][PubMed]
126. Nishibuchi M, Kumagai K, Kaper JB . 1991. Contribution of the tdh1 gene of Kanagawa phenomenon-positive Vibrio parahaemolyticus to production of extracellular thermostable direct hemolysin. Microb Pathog 11 : 453– 460.[CrossRef][PubMed]
127. Yoh M, Miwatani T, Honda T . 1992. Comparison of Vibrio parahaemolyticus hemolysin (Vp-TRH) produced by environmental and clinical isolates. FEMS Microbiol Lett 92 : 157– 161.[CrossRef][PubMed]
128. Honda T, Ni YX, Miwatani T . 1988. Purification and characterization of a hemolysin produced by a clinical isolate of Kanagawa phenomenon-negative Vibrio parahaemolyticus and related to the thermostable direct hemolysin. Infect Immun 56 : 961– 965.[PubMed]
129. Shinoda S . 2011. Sixty years from the discovery of Vibrio parahaemolyticus and some recollections. Biocontrol Sci 16 : 129– 137.[CrossRef][PubMed]
130. Kishishita M, Matsuoka N, Kumagai K, Yamasaki S, Takeda Y, Nishibuchi M . 1992. Sequence variation in the thermostable direct hemolysin-related hemolysin ( trh) gene of Vibrio parahaemolyticus. Appl Environ Microbiol 58 : 2449– 2457.[PubMed]
131. Nishibuchi M, Taniguchi T, Misawa T, Khaeomanee-Iam V, Honda T, Miwatani T . 1989. Cloning and nucleotide sequence of the gene ( trh) encoding the hemolysin related to the thermostable direct hemolysin of Vibrio parahaemolyticus. Infect Immun 57 : 2691– 2697.[PubMed]
132. Nakaguchi Y, Ishizuka T, Ohnaka S, Hayashi T, Yasukawa K, Ishiguro T, Nishibuchi M . 2004. Rapid and specific detection of tdh, trh1, and trh2 mRNA of Vibrio parahaemolyticus by transcription-reverse transcription concerted reaction with an automated system. J Clin Microbiol 42 : 4284– 4292.[CrossRef][PubMed]
133. Velazquez-Roman J, León-Sicairos N, Flores-Villaseñor H, Villafaña-Rauda S, Canizalez-Roman A . 2012. Association of pandemic Vibrio parahaemolyticus O3:K6 present in the coastal environment of northwest Mexico with cases of recurrent diarrhea between 2004 and 2010. Appl Environ Microbiol 78 : 1794– 1803.[CrossRef][PubMed]
134. Baker-Austin C, McArthur JV, Tuckfield RC, Najarro M, Lindell AH, Gooch J, Stepanauskas R . 2008. Antibiotic resistance in the shellfish pathogen Vibrio parahaemolyticus isolated from the coastal water and sediment of Georgia and South Carolina, USA. J Food Prot 71 : 2552– 2558.[CrossRef][PubMed]
135. Suffredini E, Lopez-Joven C, Maddalena L, Croci L, Roque A . 2011. Pulsed-field gel electrophoresis and PCR characterization of environmental Vibrio parahaemolyticus strains of different origins. Appl Environ Microbiol 77 : 6301– 6304.[CrossRef][PubMed]
136. González-Escalona N, Blackstone GM, DePaola A . 2006. Characterization of a Vibrio alginolyticus strain, isolated from Alaskan oysters, carrying a hemolysin gene similar to the thermostable direct hemolysin-related hemolysin gene ( trh) of Vibrio parahaemolyticus. Appl Environ Microbiol 72 : 7925– 7929.[CrossRef][PubMed]
137. Raghunath P, Maiti B, Shekar M, Karunasagar I, Karunasagar I . 2010. Clinical isolates of Aeromonas veronii biovar veronii harbor a nonfunctional gene similar to the thermostable direct hemolysin-related hemolysin ( trh) gene of Vibrio parahaemolyticus. FEMS Microbiol Lett 307 : 151– 157.[CrossRef][PubMed]
138. Suzuki N, Hashimoto S, Ishibashi M, Kim YB, Okuda J, Nishibuchi M . 1997. Levels of thermostable direct hemolysin production by Vibrio parahaemolyticus strains carrying both tdh and trh genes. Kansenshogaku Zasshi 71 : 1221– 1225. [In Japanese.][CrossRef][PubMed]
139. Bej AK, Patterson DP, Brasher CW, Vickery MC, Jones DD, Kaysner CA . 1999. Detection of total and hemolysin-producing Vibrio parahaemolyticus in shellfish using multiplex PCR amplification of tl, tdh and trh. J Microbiol Methods 36 : 215– 225.[CrossRef][PubMed]
140. Shirai H, Ito H, Hirayama T, Nakamoto Y, Nakabayashi N, Kumagai K, Takeda Y, Nishibuchi M . 1990. Molecular epidemiologic evidence for association of thermostable direct hemolysin (TDH) and TDH-related hemolysin of Vibrio parahaemolyticus with gastroenteritis. Infect Immun 58 : 3568– 3573.[PubMed]
141. Makino K, Oshima K, Kurokawa K, Yokoyama K, Uda T, Tagomori K, Iijima Y, Najima M, Nakano M, Yamashita A, Kubota Y, Kimura S, Yasunaga T, Honda T, Shinagawa H, Hattori M, Iida T . 2003. Genome sequence of Vibrio parahaemolyticus: a pathogenic mechanism distinct from that of V cholerae. Lancet 361 : 743– 749.[CrossRef][PubMed]
142. Letchumanan V, Chan KG, Lee LH . 2014. Vibrio parahaemolyticus: a review on the pathogenesis, prevalence, and advance molecular identification techniques. Front Microbiol 5 : 705.[CrossRef][PubMed]
143. Okada N, Iida T, Park KS, Goto N, Yasunaga T, Hiyoshi H, Matsuda S, Kodama T, Honda T . 2009. Identification and characterization of a novel type III secretion system in trh-positive Vibrio parahaemolyticus strain TH3996 reveal genetic lineage and diversity of pathogenic machinery beyond the species level. Infect Immun 77 : 904– 913.[CrossRef][PubMed]
144. Zhang L, Krachler AM, Broberg CA, Li Y, Mirzaei H, Gilpin CJ, Orth K . 2012. Type III effector VopC mediates invasion for Vibrio species. Cell Reports 1 : 453– 460.[CrossRef][PubMed]
145. Jones JL, Lüdeke CH, Bowers JC, Garrett N, Fischer M, Parsons MB, Bopp CA, DePaola A . 2012. Biochemical, serological, and virulence characterization of clinical and oyster Vibrio parahaemolyticus isolates. J Clin Microbiol 50 : 2343– 2352.[CrossRef][PubMed]
146. Ceccarelli D, Hasan NA, Huq A, Colwell RR . 2013. Distribution and dynamics of epidemic and pandemic Vibrio parahaemolyticus virulence factors. Front Cell Infect Microbiol 3 : 97.[CrossRef][PubMed]
147. Shrivastava S, Mande SS . 2008. Identification and functional characterization of gene components of type VI secretion system in bacterial genomes. PLoS One 3 : e2955.[CrossRef][PubMed]
148. Boyd EF, Cohen AL, Naughton LM, Ussery DW, Binnewies TT, Stine OC, Parent MA . 2008. Molecular analysis of the emergence of pandemic Vibrio parahaemolyticus. BMC Microbiol 8 : 110.[CrossRef][PubMed]
149. Izutsu K, Kurokawa K, Tashiro K, Kuhara S, Hayashi T, Honda T, Iida T . 2008. Comparative genomic analysis using microarray demonstrates a strong correlation between the presence of the 80-kilobase pathogenicity island and pathogenicity in Kanagawa phenomenon-positive Vibrio parahaemolyticus strains. Infect Immun 76 : 1016– 1023.[CrossRef][PubMed]
150. Salomon D, Klimko JA, Orth K . 2014. H-NS regulates the Vibrio parahaemolyticus type VI secretion system 1. Microbiology 160 : 1867– 1873.[CrossRef][PubMed]
151. Yu Y, Yang H, Li J, Zhang P, Wu B, Zhu B, Zhang Y, Fang W . 2012. Putative type VI secretion systems of Vibrio parahaemolyticus contribute to adhesion to cultured cell monolayers. Arch Microbiol 194 : 827– 835.[CrossRef][PubMed]
152. Hurley CC, Quirke A, Reen FJ, Boyd EF . 2006. Four genomic islands that mark post-1995 pandemic Vibrio parahaemolyticus isolates. BMC Genomics 7 : 104.[CrossRef][PubMed]
153. Xu F, Gonzalez-Escalona N, Drees KP, Sebra RP, Cooper VS, Jones SH, Whistler CA . 2017. Parallel evolution of two clades of an Atlantic-endemic pathogenic lineage of Vibrio parahaemolyticus by independent acquisition of related pathogenicity islands. Appl Environ Microbiol 83 : e01168-17.
154. Krachler AM, Mende K, Murray C, Orth K . 2012. In vitro characterization of multivalent adhesion molecule 7-based inhibition of multidrug-resistant bacteria isolated from wounded military personnel. Virulence 3 : 389– 399.[CrossRef][PubMed]
155. León-Sicairos N, Angulo-Zamudio UA, de la Garza M, Velázquez-Román J, Flores-Villaseñor HM, Canizalez-Román A . 2015. Strategies of Vibrio parahaemolyticus to acquire nutritional iron during host colonization. Front Microbiol 6 : 702.[CrossRef][PubMed]
156. Okuda J, Ishibashi M, Hayakawa E, Nishino T, Takeda Y, Mukhopadhyay AK, Garg S, Bhattacharya SK, Nair GB, Nishibuchi M . 1997. Emergence of a unique O3:K6 clone of Vibrio parahaemolyticus in Calcutta, India, and isolation of strains from the same clonal group from Southeast Asian travelers arriving in Japan. J Clin Microbiol 35 : 3150– 3155.[PubMed]