Open access peer-reviewed chapter

Community Change and Pathogenicity of Vibrio

Written By

Lixing Huang, Qiancheng Gao, Youyu Zhang, Wei Xu and Qingpi Yan

Submitted: 13 January 2021 Reviewed: 08 February 2021 Published: 11 March 2021

DOI: 10.5772/intechopen.96515

Chapter metrics overview

406 Chapter Downloads

View Full Metrics


Vibrio is a rod-shaped Gram-negative bacteria, which is widely distributed in marine and estuarine environments worldwide. It is an important component of the aquatic ecosystem and plays an important role in biogeochemical cycle. Its population dynamics are usually affected by climate and seasonal factors. Most of the Vibrios in the environment are not pathogenic, but some of them are pathogenic bacteria for human and animal, such as Vibrio cholerae, Vibrio vulnificus, Vibrio parahaemolyticus, and Vibrio anguillarum, etc., which are generally reported to be related to aquatic animal diseases and human food-borne diseases. Over the last couple of years, due to the influence of the rising seawater temperature and climate change, the incidence of diseases caused by Vibrio infection has increased significantly, which poses a great threat to human health and aquaculture. The research on pathogenic Vibrio has attracted more and more attention. The abundance and community changes of Vibrio in the environment are usually controlled by many biological and abiotic factors. The Vibrio pathogenicity is related to the virulence factors encoded by virulence genes. The process of Vibrio infecting the host and causing host disease is determined by multiple virulence factors acting together, instead of being determined by a single virulence factor. In this chapter, community changes of Vibrio, as well as the virulence factors of Vibrio and the related virulence genes of Vibiro are summarized, and their important roles in Vibrio infection are also discussed.


  • Vibrio
  • community change
  • foodborne diseases
  • pathogenicity
  • virulence factors

1. Introduction

The Vibrio belongs to the Vibrionaceae family of the Gammaproteobacteria, is a thermophilic, rod-shaped, heterotrophic Gram-negative bacterium [1]. Vibrio has genetic and metabolic diversity, and there are great phenotypic and genotypic differences among different species. It widely exists in estuaries and marine habitats all over the world and is an important part of aquatic ecosystems [2].

Vibrio usually has chemotaxis and motility, which can quickly respond to fluctuations of nutrient concentration and make use of nutrients in the environment to grow rapidly [3, 4]. In addition, Vibrio has the ability to degrade the common carbon substrates. It can decompose and utilize a variety of substrates by producing chitinase, protease, lipase and other extracellular proteases. The production and secretion of these enzymes can provide Vibrio rich nutrients unavailable for other organisms, enabling Vibrio to quickly transform from a relatively small part to a dominant bacteria in response to environmental and climate changes [5]. Vibrio plays an important role in the biogeochemical cycle, which regulates inorganic nutrients and carbon flux by fixing and re-mineralize nutrients [6].

Most Vibrio are not pathogenic, but there are several Vibrio that are pathogens of humans, fish, shellfish, or other species and can cause a range of clinical manifestations including gastroenteritis, acute diarrhea, sepsis, narcotizing soft tissue infection, high mortality in cultured aquatic animals, and, in some reported cases, human death [7, 8, 9, 10]. Vibriosis usually occurs by eating raw or under cooked seafood products, drinking contaminated water, or by direct contact with the contaminated environment through wounds [11, 12]. In the United States, the most common cause of gastroenteritis is the consumption of oysters infected or under cooked with V. parahaemolyticus [13]. According to the report of the Centers for Disease Control and Prevention (CDC) in 2006, V. parahaemolyticus is a major food-borne pathogen in the United States, and there are about 34,664 food-borne cases every year [14]. In another report, 80,000 people were infected with food-borne Vibrio annually in the United States in 2016, resulting in more than 500 hospitalizations and 100 deaths, the vast majority of which were V. vulnificus and V. parahaemolyticus [15]. Moreover, V.parahaemolyticus is a common source of food borne disease in Asian countries such as China, Japan and South Koala [7].

Aquaculture is a fast growing sector and continues to grow to meet the increasing global demand for seafood. From 2000 to 2017, aquaculture business grew by approximately 150%. China is the world’s largest aquaculture producer (accounting for 58% of global production) producing 46.8 million tons of aquaculture animals per year [9]. In order to further meet the needs of the national economy and food security, the mariculture industry in southern China has gradually developed into intensive and industrialized [16]. However, high-density farming, severe human activities and global climate change have led to frequent Vibriosis, which has posed a huge threat to human health and social and economic development [17]. Vibriosis is one of the most common bacterial diseases affecting a variety of marine fish and shellfish [18, 19]. Studies have demonstrated that the content of Vibrio in aquaculture facilities is very high, especially during the outbreak of disease. The culturable Vibrio community in the affected facilities is composed of single or few Vibrio species, including V. alginolyticus, V. parahaemolyticus, V. vulnificus and Vibrio harveyi. These species include human and animal pathogens, which can lead to high mortality of aquatic animals [20]. For example, from May 2000 to November 2003, the mortality rate of large yellow croakers reared in marine cages due to infection with V. alginolyticus and V. harveyi ranged from 30% to 40% and even as high as 80% in Zhejiang province, China [21]. In addition, wastewater from aquaculture farms is often released to the environment without treatment, potentially causing large quantities of pathogenic Vibrio to enter the environment, posing a potential threat to human health. Therefore, understanding the dynamic changes of Vibrio community and the pathogenicity of Vibrio is of great significance for the healthy development of aquaculture and reducing the impact on human public health [22, 23].


2. Dynamic changes of Vibrio community

2.1 Abundance of Vibrio

Vibrio are widely distributed in estuaries and marine environments, and mainly in nearshore areas. Vibrio generally exhibit two different growth strategies, either as a free-living form or attached to biological or non-biological surfaces, where they can co-exist with the host or cause host disease [24]. For example, some Vibrio living in squid or other organisms can be used as the source of luminescence of light-emitting organs and also an important part of the combination of biofilm and macroalgae [25].

Vibrio easily grow on conventional medium (such as seawater 2216E agar medium) and selective medium (such as thiosulfate citrate bile salt sucrose agar medium, TCBS) and can carry out a variety of metabolic activities [26]. In some studies based on culture, Vibrio can account for 10% of culturable marine bacteria [27], and the average abundance in estuaries and nearshore waters is 103 ~ 106 CFU L−1. However, in studies using non-culture methods, Vibrio population only accounts for about 1% of the total plankton bacteria in nearshore waters, and the average abundance in estuaries and nearshore waters is 104 ~ 108 16 s rRNA copies L−1 [28]. Their Vibrio abundance was found to be between 15 and 2395 CFU mL−1 in a study of tropical estuaries and coastal water in Malaysia [29]. In addition, studies have shown a high density of Vibrio on the surface and in the body of marine animals such as fish, shrimp, mollusks, corals, sponges, zooplankton, algae and seaweed [30]. For example, in a study examining the effects of aquaculture on Vibrio communities, the relative abundance of the 16SrRNA gene sequence reads 16 from seaweed samples were the highest by sequencing water, sediment, seaweed and tissue samples obtained in the aquaculture area of Hainan [9]. This is also consistent with studies describing Vibrio communities as important components of seagrass bacterial communities. These bacteria account for 25% of the culturable bacteria in seaweed off the coast of Hainan province [31].

2.2 Diversity of Vibrio

At least 110 Vibrios have been found and reported, and more may be found in the future. Among the Vibrios that have been described, several are commonly associated with human diseases, among which V. cholerae, V. parahaemolyticus, and V. vulnificus are recognized as human pathogenic bacteria, while Vibrio alginolyticus, V. anguillarum, V. harveyi, Vibrio fluvialis, Vibrio furniss, Vibrio metschnikovii, and Vibrio mimicus are primarily marine animal pathogenic bacteria but occasionally associated with human infections [32, 33, 34, 35, 36].

Vibrio usually has species-specific salinity and temperature preferences, and different kinds of Vibrio may exist in different environments. They exit from deep-sea hydrothermal vents and sediment are more than 6, 000 meters deep to seawater 10, 500 meters deep in the mariana trench [37, 38]. For example, the optimal growth temperature and salinity for Vibrio devil, first isolated from deep-sea hydrothermal vents, is 30 ~ 45 °C and 20 ~ 50 ppt, respectively [39]. The salinity-dependent Vibrio carinii is mainly present in seawater in the range of salinity from the Baltic Sea to the Mediterranean Sea [40]. Vibrio pacinii, Vibrio cyclotrophicus, Vibrio lentus, and some unnamed Vibrio have also been found at low temperatures [32].

At present, studies on the diversity of Vibrio communities in marine environments are mainly based on Vibrio isolated and cultured [41]. However, due to the low interspecific resolution of the 16S rRNA gene, the use of 16S rRNA gene similarity as a major interspecific marker for the phylogenetic relationships of Vibrios appears to have lost its effect. Multiple-locus sequence analysis (MLSA) and other novel phylogenetic markers such as the iron absorption regulatory gene fur have been used as alternative approaches [42, 43]. In order to study the diversity of environmental Vibrio, Siboni et al. first extracted DNA from seawater, and then used 16S rRNA gene primers specific to Vibrio to conduct high-throughput sequencing, thus making it possible to more intuitively and effectively explore the diversity of Vibrio communities [44]. In another study by Bei et al., the abundance and community structure of Vibrio species at different depths was studied using Vibrio-specific 16S rRNA gene high-throughput sequencing and quantitative PCR (qPCR) techniques as well as traditional culture methods [5].

2.3 The influence of environmental factors on Vibrio community

In a marine environment, abundance and community composition of Vibrio is affected by many factors, including temperature, salinity, pH, water depth, dissolved oxygen and transparency [45, 46]. Chemical factors are mainly the concentrations of inorganic and organic nutrients. In addition, biological factors such as protozoa, viruses, marine animals and algae also affect the change of Vibrio community. Therefore, under the interaction between biological and non-biological factors, the Vibrio community in the environment shows complex dynamic changes.

The abundance and community structure of Vibrio in seawater is generally considered to be related to temperature and salinity. Temperature is the most important factor affecting the change of Vibrio community. Under general conditions, the relationship between Vibrio and water temperature shows a positive correlation. Growth of Vibrio population can be observed in short-term temperature rise and long-term temperature change related to climate change [47, 48, 49]. At present, many coastal areas around the world have been reported an increase in the number of Vibrio. For example, some researchers have used continuous plankton recording equipment to show that the increase in sea temperature has caused an increase in the number of Vibrio in parts of the North Atlantic and North Sea [50]. In Peru, Alaska and the gulf of Mexico and other regions also reported that due to the increase in water temperature, some pathogenic Vibrio species began to increase [51]. Moreover, some cases of infection caused by Vibrio have also been reported to be associated with abnormally high water temperatures [52].

Salinity was the second largest factor affecting the abundance of Vibrio, and Vibrio had a positive correlation with salinity, but the relationship might also be covered by increases in temperature and nutrient concentration [53, 54]. Not only that, some studies found that short-term salinity changes do increase the concentration of Vibrio, but long-term salinity changes have no significant effect on the overall trend of Vibrio, for example, there are studies found that abundance of Vibrio is affected by salinity and chlorophyll A concentration, but only when the salinity is less than 20 ppt, the effect of salinity is significant [29]. In another study on the abundance of microbial communities in Guanabara Bay, the researchers constructed an artificial neural network that could simulate the response of environmental microbial communities to environmental parameters. The results showed that temperature had a positive correlation with the abundance of Vibrio, and salinity had a negative correlation with the abundance of Vibrio. Transparency had a positive correlation with chlorophyll concentration but had little to do with the number of Vibrio. Moreover, these physical parameters were more related to the abundance of Vibrio than in total phosphorus and total nitrogen [55]. The authors deduced that due to the high degree of eutrophication in the bay, the microbial community had reached its maximum capacity to absorb and utilize nutrients, and the growth of the microflora was no longer restricted by nutrients. On the contrary, salinity, temperature and transparency jointly determined the number of Vibrio.

Although the composition and abundance of Vibrio communities are closely related to temperature and salinity, in temperate regions, concentrations of organic and inorganic nutrients and phytoplankton communities appear to be more important drivers of seasonal changes in Vibrio communities because annual changes in temperature are not significant.

In a study of wetlands in Macchiatonda Regional Nature Reserve, it was found that the CFU abundance of TCBS depended on temperature and salinity, and the effect of temperature was greater than that of salinity (27% and 20%, respectively), but since temperature and salinity accounted for only 40% of the total CFU abundance, other environmental and biological factors had to play a role in driving Vibrio abundance in the system of the region [32]. In another ten-year study of the mouth of the Newz River in North Carolina, the United States, it seems that similar views have been confirmed. During the study, the temperature of the estuary did not change significantly, but the number of some Vibrios closely related to the temperature increased. The salinity of the estuary showed a trend of increasing to the highest and decreasing during the study. The increase of the number of Vibrio in the estuary had to be in conformity with the decrease in salinity. When the salinity increased, the number of Vibrios in the mouth of the river increased. Some specific Vibrio, such as V. vulnificus, had almost declined to undetectable levels, and the final conclusion was that the concentration of Vibrio in the area appeared to be independent of changes in the three factors commonly used to predict Vibrio abundance, including salinity, temperature, and dissolved oxygen. Although the overall abundance of Vibrio was on the rise, the number of some potential pathogenic species was decreasing, and the concentration of Vibrio in the estuaries was predicted to be related to nitrogen and carbon in the environment [2]. In addition, studies have shown that ammonium radical promotes the growth of Vibrio, while silicic acid and phosphate have opposite effects on Vibrio population [56]. Dissolved organic carbon (DOC) has a strong impact on the ecology of Vibrio. DOC provides a large amount of nutrients needed for Vibrio living in estuarine and marine habitats. Vibrio can absorb, metabolize and produce organic matter, thus changing its chemical properties and bioavailability [57]. Therefore, in temperate regions where the temperature is relatively stable, factors other than physical parameters such as temperature and salinity may play a more important role. However, when the degree of nutrition is high and the microbial community has reached the maximum capacity to absorb and utilize nutrition, physical factors are more relevant to the abundance of Vibrio.

Dissolved oxygen is an important hydrological parameter, which affects the number of Vibrio bacteria by affecting their metabolism. Due to hypoxia, the Vibrio population will switch from breathing mode to fermentation mode [58]. The abundance of free-living and particulate-related fractions of Vibrio was negatively correlated with dissolved oxygen (48.7% ~ 105.8% saturation) in the coastal area of georgia, USA [59]. A negative correlation between Vibrio abundance and dissolved oxygen (5 ~ 11 mg L−1) was found in the North Carolina estuary [60]. In addition, a study on Yongle Blue Cave in Sansha, Hainan, China found that in the deepest Blue Cave in the world, due to the strong stratification limiting the vertical exchange of oxygen, the water body was divided into an upper aerobic zone and a lower anoxic zone. The strong DO gradient resulted in no significant correlation between Vibrio abundance and temperature, but Vibrio abundance was very high at a depth of 100 m (the interface between aerobic and anoxic) [5].

In addition to physical factors, biological factors also play an important role in affecting changes in the Vibrio community. The virus has a strong lethal effect on Vibrio and can greatly affect the change of Vibrio community. Some researchers have identified a virus with a wide host range from infected Vibrio, which can kill 34 Vibrio strains of four species [61]. For some special species, changes in biological factors may have a stronger effect on their abundance than non-biological parameters [62, 63]. Recently, it has been proved that there is a significant correlation between the abundance of particle-associated Vibrio and the community composition of phytoplankton, and it is speculated that this may be related to the bioavailability of dissolved organic matter released from phytoplankton [64].

Finally, Vibrio can enter a viable but non-culturable state (VBNC) under adverse environmental conditions (such as oligotrophic, excessively high or low temperature, high salt, extreme pH, and sunlight radiation). This physiological state is reversible, and when the conditions become favorable again, the pathogen will recover [65]. The cells could still survive in this dormant state, but it could not be detected by the traditional culture method, which might show a higher resistance to exogenous stress and maintain the active virulence factors [66]. However, conditions for Vibrio to enter “recovery” from “dormancy” are not completely clear.


3. Pathogenicity of Vibrio

Vibrio is usually reported being related to food-borne diseases and aquaculture diseases. Diseases or even death of aquatic animals caused by Vibrio infection have been reported worldwide and are showing an increasing trend [7, 11, 18, 67]. Therefore, Vibriosis has caused significant impacts on human health and the development of aquaculture [68, 69, 70]. The pathogenicity of Vibrio is determined by multiple virulence factors encoded by its virulence genes [71, 72, 73, 74]. Vibrio infects and destroys the host through a series of processes, including adhesion, invasion, immune escape, in vivo proliferation and production of toxins [46]. Vibrio mainly includes adhesion factor, the capsule and polysaccharide, cytotoxin and other virulence factors [75]. Therefore, infection and pathogenesis of Vibrio are not completed by a single virulence factor, but the result of the combined action of multiple virulence factors.

3.1 Adhesion factor

Adhesion is the prerequisite for pathogenic bacteria to cause disease to the body infection, and it is of great significance in invading the host and effectively exerting the virulence [76]. Adhesion is mainly achieved by adhesion factors that specifically recognize and bind to host cells, the ability of Vibrio to adhere to and form biofilm on the surfaces of organisms and non-organisms can enhance the virulence and pathogenicity of Vibrio [77]. Moreover, adhesion is strongly related to the biofilm formation ability, movement ability and quorum sensing of bacterial [78].

Adhesion factor is a kind of macromolecular substance that can make pathogenic bacteria adhere to the surface of eukaryotic cells, and it plays an important role in the host infection process of Vibrio. Vibrio has a variety of adhesin, such as fimbriae, cilia, outer membrane protein (OMP), lipopolysaccharide (LPS), extracellular polysaccharide, etc. Among them, fimbriae and cilia belong to fimbriae adhesin, while OMP, LPS, and extracellular polysaccharides belong to non-pilin adhesin [79]. The exposure of OMP to the bacterial surface is a unique and important component of the outer membrane of Gram-negative bacteria, which plays an important role in maintaining the outer membrane structure, ensuring the transport of substances, and stimulating the body to produce antibodies and cytokines. It has been found that the outer membrane protein is an important pathogenic factor closely related to the process of bacterial adhesion and iron uptake [80]. LPS is a lipopolysaccharide substance located in the outermost layer of the cell wall of Gram-negative bacteria. It is not only the main component of the cell wall of Gram-negative bacteria, but also the material basis for the endotoxin of the virulence factor of Gram-negative pathogens [81]. In Vibrio pathogens (such as V. anguillarum, V. vulnificus, V. cholerae, V. mimicus, V. parahaemolyticus, etc.), LPS has been proven to be an important pathogenic factor [82].

Although Vibrio has a variety of adhesion factors, previous studies on the adhesion of Vibrio generally focused on flagellum, and some researchers proposed that flagellum plays an irreplaceable role in the adhesion process of bacteria-infected host [83]. According to the location of the flagellum, the flagellum can be divided into two types: terminal flagellum and peri-flagellum. Belas investigated the differences in the adsorption characteristics of Vibrio with different types of flagellum on chitin, and found that peri-flagellum had a stronger affinity for chitin than terminal flagellum [84]. The adhesion of V. alginolyticus to the epidermal mucus of Sparus macrocephalus was studied by Bordas, which also proved this viewpoint [85]. In addition, studies have found that pili seems to have a strong correlation with the pathogenicity of Vibrio. Wright first found in 1989, most clinical isolates of V. vulnificus have pili, while environmental isolates lack pili [86]. Analysis of pili protein gene expression during infection indicated that the pili protein expression of the strong strain was higher than that of the weak strain [87]. Moreover, the mobility of the strain was also one of the main factors affecting the adhesion. Kogure found that under the condition of having flagella at the same time, strains with mobility showed faster and stronger adhesion than the strains without mobility [88].

3.2 Capsular and polysaccharide

After entering the host, bacteria usually activate the host immune system to cause a series of immune responses to eliminate pathogens [89]. In order to survive and reproduce in the host, bacteria must adopt a series of strategies to improve their viability and virulence in the host as well as their resistance to phagocytosis and antibiotics.

The correlation between the capsular and polysaccharide and virulence has been confirmed [90]. The capsule encapsulated on the surface of bacteria is a dense, high molecular weight capsule that plays a major role in evading the host’s immune defense. The encapsulated pathogen shows strong resistance to phagocytosis and complement-mediated lethality. Studies have shown that organisms with capsular polysaccharides are more likely to survive in serum, that isolates expressing opaque colonies are more resistant to serum than translucent isolates, and there are differences in colony characteristics between seafood isolates and clinical isolates. Clinical isolates were more resistant to serum complement proteins than environmental isolates, and the clinical genotype had a consistent survival advantage when exposed to serum [91, 92, 93]. In addition, the formation of biofilm will also promote the adhesion of pathogens to the host, coordinate the quorum sensing between bacteria, and improve the resistance of pathogens to antibiotics, playing a major role in the escape of pathogens from host immunity.

3.3 Cytotoxins

Cytotoxic is the main killer factor of pathogens in the process of attacking the host. Toxins secreted by Vibrio can be divided into endotoxin and exotoxin. Endotoxin is the lipid part of lipopolysaccharide released after cell death, and the exotoxin is secreted out of cells to cause damage to the host. At present, the toxins produced by Vibrio have been studied in depth, and the expression of many virulence factors is related to the pathogenicity of Vibrio, including: Thermostable direct hemolysin (TDH), TDH-related hemolysin (TRH), V. vulnificus cytolytic toxin (VVC), cholera toxin (CT), and zonulaoccludens toxin (Zot).

V. parahaemolyticus is one of the main bacterial isolates of food poisoning caused by seafood contamination and is usually associated with outbreaks of foodborne diseases [11]. The thermostable direct hemolysin (TDH) and TDH-related hemolysin (TRH) encoded by the tdh and trh genes are considered to be the main virulence factors of V. parahaemolyticus. TDH has a variety of biological activities, such as hemolytic activity, cytotoxicity, cardiotoxicity and enterictoxicity. TDH is a perforated toxin, and its toxic mechanism is to create pores with a diameter of 0 ∼ 2 nm on the erythrocyte membrane, among which the larger pores can make the water and ions in the cells flow out of the cell membrane, and changes in these ion fluxes in the intestine are also the main cause of diarrhea [94, 95]. TRH is a thermolabile toxin, which is similar to TDH in immunology, and can also activate chloride channels and cause changes in ion flux [96]. TDH and TRH share approximately 70% homology [97], and these two genes are considered to be the most important virulence markers of V. parahaemolyticus and are commonly used for virulence testing of V. parahaemolyticus [98].

V. vulnificus is a conditionally pathogenic human pathogen, which can cause severe wound infection, acute gastroenteritis and life-threatening septicemia. In susceptible or immunocompromised individuals, the mortality rate exceeds 50% [99]. VVC encoded by VvhA gene of V. vulnificus is the key virulence factor of V. vulnificus, which mainly plays a role through two mechanisms: cytolysis and apoptosis induction [100]. VVC has species specificity in V. vulnificus, which is the only exotoxin that can be secreted out of cells, and belongs to cholesterol-dependent cytolysin of pore-forming protein family [101]. The cytotoxic mechanism of cytotoxin is that it combines with non-esterified cholesterol on cell membrane and aggregates on the cell surface, which makes the cell membrane form a channel and leads to the outflow of intracellular potassium ions, which leads to the rupture of colloid permeable cells. The main mechanism of apoptosis induced by cytotoxin is related to mitochondria. Cytotoxin can lead to the production of mitochondrial reactive oxygen species (ROS) in intestinal epithelial cells, and then lead to cell necrosis and apoptosis [102].

V. cholerae has caused several epidemics in history. Cholera toxin (CT) is the main pathogenic factor of O1/O139 V. cholerae, which can cause serious damage to intestinal cell function and lead to cholera watery secretory diarrhea [103]. CT is encoded by ctxA and ctxB. These genes are encoded by CTXΦ of lysogenic filamentous phage and can be transferred between virulent and non-virulent strains [104]. zot is also encoded by lysogenic filamentous bacteriophage CTXΦ [105], and its encoded zona-linked toxin (ZOT) is the second virulence index of V. cholerae, which can make mucosal cells adhere together, maintain the tight connection structure of mucosal integrity and increase the permeability of intestinal mucosa [106]. Except as a cytotoxin, Zot seems to be related to the assembly of CTX phage in structure and function. Zot gene has sequence homology with the coat protein gene, which is probably the coat protein of CTX Φ. This indicates that it may have dual functions [107].

3.4 Other virulence factors

In addition to secreting toxins, some pathogenic bacteria can secrete a variety of extracellular products, which are also the main factors causing host diseases. For example, Balebona and Morinigo discovered in 1995 that the extracellular products of V. alginolyticus have various enzyme activities such as caseinase, gelatinase, amylase, phospholipase, collagenase, etc., and these extracellular products have strong toxicity to fish cells, which can dissolve fish cells and cause fish death [108]. Balebona et al. infected fish by intramuscular injection with extracellular protease. After 6 h, it was observed that the injected extracellular products were lysed, which could lead to fish death in 24 ~ 72 h [109]. Lee et al. found that alkaline serine protease produced by V. alginolyticus can reduce thrombin in prawn plasma and prevent hemolymph from agglutinating, which is one of the main lethal factors secreted by V. alginolyticus. V. vulnificus metalloproteinases (VVP) is a kind of zinc ion-dependent protease with hemolysis. Miyoshi et al. studies have proved that VVP can enhance vascular permeability, destroy the basement membrane, cause bleeding reaction, cause cell and tissue damage, and eventually develop into sepsis [110].

Iron, as an indispensable trace element, is also an important component of various cellular enzymes, and plays an important role in the growth, reproduction, pathogenicity and cellular metabolism of pathogenic bacteria [111]. The iron carrier of Vibrio is an important pathogenic factor, and the iron uptake system mediated by it plays a very important role in bacterial growth and host colonization. Under the condition of lack of iron, the strain will produce a chelation agent iron carrier with high affinity for heme iron ions and low molecular weight, and the iron absorbed from transferrin and lactoferrin will be transported to bacterial cells for its own use through the receptor [112].


4. Conclusion

Vibrio, as a kind of human and animal pathogen, exists widely in the world, and its increasing number and pathogenicity are great challenges to human public health and healthy aquaculture. The changes of Vibrio community in the environment are related to abiotic factors (temperature, salinity, pH, water depth, dissolved oxygen, transparency, nutrient concentration, etc.) and biological factors (protozoa, viruses, marine animals and algae, etc.), among which temperature and salinity are considered to be the most important factors affecting the changes of Vibrio community, but in temperate regions where salinity and temperature are relatively stable, nutrient concentration and phytoplankton community contribute more to the changes of Vibrio community. In recent years, with the outbreak of Vibrio in some areas caused by climate change and rising seawater temperature, the number of some pathogenic Vibrio began to increase. The pathogenicity of Vibrio is related to virulence factors encoded by virulence genes (adhesion factors, cytotoxins, extracellular enzymes, capsular polysaccharides, iron uptake system, etc.), and different virulence factors play different roles in the infection process. In this chapter, the influencing factors of Vibrio community change and various virulence factors of Vibrio in the process of infecting the host were summarized, in order to provide reference and help for human public health and aquaculture industry.


  1. 1. Thompson FL, Iida T, Swings J. Biodiversity of vibrios. Microbiol Mol Biol Rev, 2004,68(3): 403-431
  2. 2. Froelich B, Gonzalez R, Blackwood D, et al. Decadal monitoring reveals an increase in Vibrio spp. concentrations in the Neuse River Estuary, North Carolina, USA. PLoS One, 2019,14(4): e215254
  3. 3. Westrich JR, Griffin DW, Westphal DL, et al. Vibrio Population Dynamics in Mid-Atlantic Surface Waters during Saharan Dust Events. Frontiers in Marine Science, 2018,5
  4. 4. Huang L, Huang L, Zhao L, et al. The regulation of oxidative phosphorylation pathway on Vibrio alginolyticus adhesion under adversities. MicrobiologyOpen, 2019
  5. 5. Bei L, Jiwen L, Shun Z, et al. Vertical variation in Vibrio community composition in Sansha Yongle Blue Hole and its ability to degrade macromolecules. Marine Life Science & Technology, 2020,2(1)
  6. 6. Zeng J, Lin Y, Zhao D, et al. Seasonality overwhelms aquacultural activity in determining the composition and assembly of the bacterial community in Lake Taihu, China. Sci Total Environ, 2019,683: 427-435
  7. 7. Dahanayake PS, Silva BCJD, Hossain S, et al. Occurrence, virulence factors, and antimicrobial susceptibility patterns of Vibrio spp. isolated from live oyster ( Crassostrea gigas ) in Korea. Journal of food safety, 2018,38(5): e12490
  8. 8. Ford CL, Powell A, Lau D, et al. Isolation and characterization of potentially pathogenic Vibrio species in a temperate, higher latitude hotspot. Environ Microbiol Rep, 2020,12(4): 424-434
  9. 9. Möller L, Kreikemeyer B, Luo Z, et al. Impact of coastal aquaculture operation systems in Hainan island (China) on the relative abundance and community structure of Vibrio in adjacent coastal systems. Estuarine, coastal and shelf science, 2020,233: 106542
  10. 10. Huang L, Guo L, Xu X, et al. The role of rpoS in the regulation of Vibrio alginolyticus virulence and the response to diverse stresses. J Fish Dis, 2019,42(5): 703-712
  11. 11. Jeamsripong S, Khant W, Chuanchuen R. Distribution of phenotypic and genotypic antimicrobial resistance and virulence genes in Vibrio parahaemolyticus isolated from cultivated oysters and estuarine water. FEMS Microbiol Ecol, 2020,96(8)
  12. 12. Zuo Y, Zhao L, Xu X, et al. Mechanisms underlying the virulence regulation of new Vibrio alginolyticus ncRNA Vvrr1 with a comparative proteomic analysis. Emerg Microbes Infect, 2019,8(1): 1604-1618
  13. 13. Daniels NA, Mackinnon L, Bishop R, et al. Vibrio parahaemolyticus Infections in the United States, 1973-1998. The Journal of infectious diseases, 2000,181(5): 1661-1666
  14. 14. Scallan E, Hoekstra RM, Angulo FJ, et al. Foodborne illness acquired in the United States--major pathogens. Emerg Infect Dis, 2011,17(1): 7-15
  15. 15. FoodNet 2015 Annual Foodborne Illness Surveillance Report[R]
  16. 16. Hong W, Zhang Q . Review of captive bred species and fry production of marine fish in China. Aquaculture, 2003,227(1): 305-318
  17. 17. Xu X, Huang L, Su Y, et al. The complete genome sequence of Vibrio aestuarianus W-40 reveals virulence factor genes. Microbiologyopen, 2018,7(3): e568
  18. 18. Deng Y, Xu L, Chen H, et al. Prevalence, virulence genes, and antimicrobial resistance of Vibrio species isolated from diseased marine fish in South China. Sci Rep, 2020,10(1): 14329
  19. 19. Guo L, Huang L, Su Y, et al. secA, secD, secF, yajC, and yidC contribute to the adhesion regulation of Vibrio alginolyticus. Microbiologyopen, 2018,7(2): e551
  20. 20. Huang L, Wang L, Lin X, et al. mcp, aer, cheB, and cheV contribute to the regulation of Vibrio alginolyticus (ND-01) adhesion under gradients of environmental factors. Microbiologyopen, 2017,6(6)
  21. 21. Jin S, Wang G, Zhao Q , et al. Epidemiology of vibriosis in large yellow croaker Pseudosciaena crocea (richardson) in marine cage culture[Z]. 2005: 24, 17-19
  22. 22. Sung HH, Hsu SF, Chen CK, et al. Relationships between disease outbreak in cultured tiger shrimp (Penaeus monodon) and the composition of Vibrio communities in pond water and shrimp hepatopancreas during cultivation. Aquaculture, 2001,192(2-4): 101-110
  23. 23. Al-Harbi AH, Uddin N. Bacterial diversity of tilapia ( Oreochromis niloticus ) cultured in brackish water in Saudi Arabia. Aquaculture, 2005,250(3-4): 566-572
  24. 24. Reen FJ, Almagro-Moreno S, Ussery D, et al. The genomic code: inferring Vibrionaceae niche specialization. Nat Rev Microbiol, 2006,4(9): 697-704
  25. 25. Fidopiastis PM, Boletzky SV, Ruby EG. A new niche for Vibrio logei, the predominant light organ symbiont of squids in the genus Sepiola. J Bacteriol, 1998,180(1): 59-64
  26. 26. Thompson FL, Brian A, Jean S. The Biology of Vibrios[M]. ASM Press, 2006
  27. 27. Eilers H, Pernthaler J, Glockner FO, et al. Culturability and In situ abundance of pelagic bacteria from the North Sea. Appl Environ Microbiol, 2000,66(7): 3044-3051
  28. 28. Thompson JR, Polz MF. Dynamics of Vibrio Populations and Their Role in Environmental Nutrient Cycling[M]. John Wiley & Sons, Ltd, 2014
  29. 29. Wong YY, Lee CW, Bong CW, et al. Environmental control of Vibrio spp. abundance and community structure in tropical waters. FEMS Microbiol Ecol, 2019,95(11)
  30. 30. Liu W, Huang L, Su Y, et al. Contributions of the oligopeptide permeases in multistep of Vibrio alginolyticus pathogenesis. Microbiologyopen, 2017,6(1)
  31. 31. Jiang YF, Ling J, Wang YS, et al. Cultivation-dependent analysis of the microbial diversity associated with the seagrass meadows in Xincun Bay, South China Sea. Ecotoxicology, 2015,24(7-8): 1540-1547
  32. 32. Matteucci G, Schippa S, Di Lallo G, et al. Species diversity, spatial distribution, and virulence associated genes of culturable vibrios in a brackish coastal Mediterranean environment. Annals of microbiology, 2015,65(4): 2311-2321
  33. 33. Huang L, Huang L, Yan Q , et al. The TCA Pathway is an Important Player in the Regulatory Network Governing Vibrio alginolyticus Adhesion Under Adversity. Front Microbiol, 2016,7: 40
  34. 34. Wang L, Huang L, Su Y, et al. Involvement of the flagellar assembly pathway in Vibrio alginolyticus adhesion under environmental stresses. Front Cell Infect Microbiol, 2015,5: 59
  35. 35. Huang L, Hu J, Su Y, et al. Genome-Wide Detection of Predicted Non-coding RNAs Related to the Adhesion Process in Vibrio alginolyticus Using High-Throughput Sequencing. Front Microbiol, 2016,7: 619
  36. 36. Luo G, Huang LX, Su YQ , et al. flrA, flrB and flrC regulate adhesion by controlling the expression of critical virulence genes in Vibrio alginolyticus. Emerging Microbes & Infections, 2016
  37. 37. Liu J, Zheng Y, Lin H, et al. Proliferation of hydrocarbon-degrading microbes at the bottom of the Mariana Trench. Microbiome, 2019,7(1): 47
  38. 38. Hasan NA, Grim CJ, Lipp EK, et al. Deep-sea hydrothermal vent bacteria related to human pathogenic Vibrio species. Proc Natl Acad Sci U S A, 2015,112(21): E2813-E2819
  39. 39. Raguenes G, Christen R, Guezennec J, et al. Vibrio diabolicus sp. nov., a new polysaccharide-secreting organism isolated from a deep-sea hydrothermal vent polychaete annelid, Alvinella pompejana. Int J Syst Bacteriol, 1997,47(4): 989-995
  40. 40. Thompson, FL. Vibrio kanaloae sp. nov., Vibrio pomeroyi sp. nov. and Vibrio chagasii sp. nov., from sea water and marine animals. INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, 2003,53(3)
  41. 41. Amin AK, Feng G, Al-Saari N, et al. The First Temporal and Spatial Assessment of Vibrio Diversity of the Surrounding Seawater of Coral Reefs in Ishigaki, Japan. Front Microbiol, 2016,7: 1185
  42. 42. Machado H, Gram L. The fur gene as a new phylogenetic marker for Vibrionaceae species identification. Appl Environ Microbiol, 2015,81(8): 2745-2752
  43. 43. Pascual J, Macian MC, Arahal DR, et al. Multilocus sequence analysis of the central clade of the genus Vibrio by using the 16S rRNA, recA, pyrH, rpoD, gyrB, rctB and toxR genes. Int J Syst Evol Microbiol, 2010,60(Pt 1): 154-165
  44. 44. Siboni N, Balaraju V, Carney R, et al. Spatiotemporal Dynamics of Vibrio spp. within the Sydney Harbour Estuary. Front Microbiol, 2016,7: 460
  45. 45. Kong W, Huang L, Su Y, et al. Investigation of possible molecular mechanisms underlying the regulation of adhesion in Vibrio alginolyticus with comparative transcriptome analysis. Antonie Van Leeuwenhoek, 2015,107(5): 1197-1206
  46. 46. Huang L, Hu J, Su Y, et al. Identification and characterization of three Vibrio alginolyticus non-coding RNAs involved in adhesion, chemotaxis, and motility processes. Front Cell Infect Microbiol, 2015,5: 56
  47. 47. Baker-Austin C, Trinanes JA, Salmenlinna S, et al. Heat Wave–Associated Vibriosis, Sweden and Finland, 2014. Emerging infectious diseases, 2016,22(7): 1216-1220
  48. 48. Baker-Austin C, Trinanes JA, Taylor NGH, et al. Emerging Vibrio risk at high latitudes in response to ocean warming. Nature Climate Change, 2013,3(1): 73-77
  49. 49. Sterk A, Schets FM, Husman AMDR, et al. Effect of Climate Change on the Concentration and Associated Risks of Vibrio Spp. in Dutch Recreational Waters. Risk Analysis, 2015,35(9): 1717-1729
  50. 50. Vezzulli L, Grande C, Reid PC, et al. Climate influence on Vibrio and associated human diseases during the past half-century in the coastal North Atlantic. Proc Natl Acad Sci U S A, 2016,113(34): E5062-E5071
  51. 51. Martinez-Urtaza J, Bowers JC, Trinanes J, et al. Climate anomalies and the increasing risk of Vibrio parahaemolyticus and Vibrio vulnificus illnesses. Food Research International, 2010,43(7): 1780-1790
  52. 52. Baker-Austin C, Trinanes JA, Salmenlinna S, et al. Heat Wave-Associated Vibriosis, Sweden and Finland, 2014. Emerg Infect Dis, 2016,22(7): 1216-1220
  53. 53. Oberbeckmann S, Fuchs BM, Meiners M, et al. Seasonal dynamics and modeling of a Vibrio community in coastal waters of the North Sea. Microb Ecol, 2012,63(3): 543-551
  54. 54. Hsieh JL, Fries JS, Noble RT. Dynamics and predictive modelling of Vibrio spp. in the Neuse River Estuary, North Carolina, USA. Environ Microbiol, 2008,10(1): 57-64
  55. 55. Coutinho FH, Thompson CC, Cabral S, et al. Modelling the influence of environmental parameters over marine planktonic microbial communities using artificial neural networks. Sci Total Environ, 2019,677: 205-214
  56. 56. Asplund ME, Rehnstam-Holm AS, Atnur V, et al. Water column dynamics of Vibrio in relation to phytoplankton community composition and environmental conditions in a tropical coastal area. Environ Microbiol, 2011,13(10): 2738-2751
  57. 57. Takemura AF, Chien DM, Polz MF. Associations and dynamics of Vibrionaceae in the environment, from the genus to the population level. Front Microbiol, 2014,5: 38
  58. 58. Garcia-Amado MA, Bozo-Hurtado L, ASTOR Y, et al. Denaturing gradient gel electrophoresis analyses of the vertical distribution and diversity of Vibrio spp. populations in the Cariaco Basin. FEMS Microbiol Ecol, 2011,77(2): 347-356
  59. 59. Turner JW, Good B, Cole D, et al. Plankton composition and environmental factors contribute to Vibrio seasonality. ISME J, 2009,3(9): 1082-1092
  60. 60. Blackwell KD, Oliver JD. The ecology of Vibrio vulnificus, Vibrio cholerae, and Vibrio parahaemolyticus in North Carolina estuaries. J Microbiol, 2008,46(2): 146-153
  61. 61. Kauffman KM, Hussain FA, Yang J, et al. A major lineage of non-tailed dsDNA viruses as unrecognized killers of marine bacteria. Nature, 2018,554(7690): 118-122
  62. 62. Davis B, Jacobs JM, Davis MF, et al. Environmental Determinants of Vibrio parahaemolyticus in the Chesapeake Bay. Appl Environ Microbiol, 2017,83(21)
  63. 63. Kopprio GA, Streitenberger ME, Okuno K, et al. Biogeochemical and hydrological drivers of the dynamics of Vibrio species in two Patagonian estuaries. Sci Total Environ, 2017,579: 646-656
  64. 64. Main CR, Salvitti LR, Whereat EB, et al. Community-Level and Species-Specific Associations between Phytoplankton and Particle-Associated Vibrio Species in Delaware's Inland Bays. Appl Environ Microbiol, 2015,81(17): 5703-5713
  65. 65. Colwell RR. Viable but Not Cultivable Bacteria[M]. 2009
  66. 66. Li L, Mendis N, Trigui H, et al. The importance of the viable but non-culturable state in human bacterial pathogens. Front Microbiol, 2014,5: 258
  67. 67. Yang L, Wang Y, Yu P, et al. Prophage-Related Gene VpaChn25_0724 Contributes to Cell Membrane Integrity and Growth of Vibrio parahaemolyticus CHN25. Frontiers in cellular and infection microbiology, 2020,10: 595709
  68. 68. Biswas S, Chouhan OP, Bandekar D. Diguanylate Cyclases in Vibrio cholerae: Essential Regulators of Lifestyle Switching. Front Cell Infect Microbiol, 2020,10: 582947
  69. 69. Qin Z, Yang X, Chen G, et al. Crosstalks Between Gut Microbiota and Vibrio Cholerae. Front Cell Infect Microbiol, 2020,10: 582554
  70. 70. Perez-Reytor D, Pavon A, Lopez-Joven C, et al. Analysis of the Zonula occludens Toxin Found in the Genome of the Chilean Non-toxigenic Vibrio parahaemolyticus Strain PMC53.7. Front Cell Infect Microbiol, 2020,10: 482
  71. 71. Schroeder M, brooks BD, Brooks AE. The Complex Relationship between Virulence and Antibiotic Resistance. Genes (Basel), 2017,8(1)
  72. 72. Ramamurthy T, Nandy RK, Mukhopadhyay AK, et al. Virulence Regulation and Innate Host Response in the Pathogenicity of Vibrio cholerae. Front Cell Infect Microbiol, 2020,10: 572096
  73. 73. Kumar A, Das B, Kumar N. Vibrio Pathogenicity Island-1: The Master Determinant of Cholera Pathogenesis. Front Cell Infect Microbiol, 2020,10: 561296
  74. 74. Wu C, Zhao Z, Liu Y, et al. Type III Secretion 1 Effector Gene Diversity Among Vibrio Isolates From Coastal Areas in China. Front Cell Infect Microbiol, 2020,10: 301
  75. 75. Wu HJ, Wang AH, Jennings MP. Discovery of virulence factors of pathogenic bacteria. Curr Opin Chem Biol, 2008,12(1): 93-101
  76. 76. Wilson. Bacterial adhesion to host tissues. 2002
  77. 77. Efstathios G, Even H, Micka LD, et al. Intra- and inter-species interactions within biofilms of important foodborne bacterial pathogens. Frontiers in Microbiology, 2015,6(841): 841
  78. 78. Thakur P, Chawla R, Tanwar A, et al. Attenuation of adhesion, quorum sensing and biofilm mediated virulence of carbapenem resistant Escherichia coli by selected natural plant products. Microb Pathog, 2016,92: 76-85
  79. 79. Wang XH, Leung KY. Biochemical characterization of different types of adherence of Vibrio species to fish epithelial cells. Microbiology (Reading), 2000,146 ( Pt 4): 989-998
  80. 80. Bricknell IR, King JA, Bowden TJ, et al. Duration of protective antibodies, and the correlation with protection in Atlantic salmon (Salmo salar L.), following vaccination with an Aeromonas salmonicida vaccine containing iron-regulated outer membrane proteins and secretory polysaccharide. Fish & Shellfish Immunology, 1999,9(2): 139-151
  81. 81. Hisatsune K, Kiuye A, Kondo S. A comparative study of the sugar composition of O-antigenic lipopolysaccharides isolated from Vibrio alginolyticus and Vibrio parahaemolyticus. Microbiol Immunol, 1981,25(2): 127-136
  82. 82. Milton DL, Norqvist A, Wolf-Watz H. Sequence of a novel virulence-mediating gene, virC, from Vibrio anguillarum. Gene, 1995,164(1): 95-100
  83. 83. Meadows PS. The attachment of bacteria to solid surfaces. Archiv Für Mikrobiologie, 1971,75(4): 374-381
  84. 84. Belas MR, Colwell RR. Adsorption kinetics of laterally and polarly flagellated Vibrio. J Bacteriol, 1982,151(3): 1568-1580
  85. 85. Bordas MA, Balebona MC, Zorrilla I, et al. Kinetics of adhesion of selected fish-pathogenic Vibrio strains of skin mucus of gilt-head sea bream (Sparus aurata L.). Appl Environ Microbiol, 1996,62(10): 3650-3654
  86. 86. Wright AC, Simpson LM, Oliver JD, et al. Phenotypic evaluation of acapsular transposon mutants of Vibrio vulnificus. Infect Immun, 1990,58(6): 1769-1773
  87. 87. Kim IH, Kim BS, Lee KS, et al. Identification of virulence factors in vibrio vulnificus by comparative transcriptomic analyses between clinical and environmental isolates using cDNA microarray. J Microbiol Biotechnol, 2011,21(12): 1228-1235
  88. 88. Kogure K, Ikemoto E, Morisaki H. Attachment of Vibrio alginolyticus to glass surfaces is dependent on swimming speed. J Bacteriol, 1998,180(4): 932-937
  89. 89. Sperandio B, Fischer N, Sansonetti P J. Mucosal physical and chemical innate barriers: Lessons from microbial evasion strategies. Semin Immunol, 2015,27(2): 111-118
  90. 90. Wright AC, Simpson L M, Oliver JD, et al. Phenotypic evaluation of acapsular transposon mutants of Vibrio vulnificus. Infect Immun, 1990,58(6): 1769-1773
  91. 91. Williams TC, Ayrapetyan M, Ryan H, et al. Serum Survival of Vibrio vulnificus: Role of Genotype, Capsule, Complement, Clinical Origin, and in Situ Incubation. Pathogens, 2014,3(4): 822-832
  92. 92. Johnson DE, Calia FM, Musher DM, et al. Resistance of Vibrio vulnificus to serum bactericidal and opsonizing factors: relation to virulence in suckling mice and humans. J Infect Dis, 1984,150(3): 413-418
  93. 93. Garrett SB, Garrison-schilling KL, Cooke JT, et al. Capsular polysaccharide production and serum survival of Vibrio vulnificus are dependent on antitermination control by RfaH. FEBS Lett, 2016,590(24): 4564-4572
  94. 94. Matsumoto C, Okuda J, Ishibashi M, et al. Pandemic spread of an O3:K6 clone of Vibrio parahaemolyticus and emergence of related strains evidenced by arbitrarily primed PCR and toxRS sequence analyses. J Clin Microbiol, 2000,38(2): 578-585
  95. 95. Honda T, Ni Y, Miwatani T, et al. The thermostable direct hemolysin of Vibrio parahaemolyticus is a pore-forming toxin. Can J Microbiol, 1992,38(11): 1175-1180
  96. 96. Takahashi A, Kenjyo N, Imura K, et al. Cl(−) secretion in colonic epithelial cells induced by the Vibrio parahaemolyticus hemolytic toxin related to thermostable direct hemolysin. Infect Immun, 2000,68(9): 5435-5438
  97. 97. Honda T, Ni YX, Miwatani T. 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, 1988,56(4): 961-965
  98. 98. Letchumanan V, Pusparajah P, Tan LT, et al. Occurrence and Antibiotic Resistance of Vibrio parahaemolyticus from Shellfish in Selangor, Malaysia. Front Microbiol, 2015,6: 1417
  99. 99. Jones MK, Oliver JD. Vibrio vulnificus: disease and pathogenesis. Infect Immun, 2009,77(5): 1723-1733
  100. 100. Gavin HE, Beubier NT, Satchell KJ. The Effector Domain Region of the Vibrio vulnificus MARTX Toxin Confers Biphasic Epithelial Barrier Disruption and Is Essential for Systemic Spread from the Intestine. PLoS Pathog, 2017,13(1): e1006119
  101. 101. Jeong HG, Satchell KJ. Additive function of Vibrio vulnificus MARTX(Vv) and VvhA cytolysins promotes rapid growth and epithelial tissue necrosis during intestinal infection. PLoS Pathog, 2012,8(3): e1002581
  102. 102. Lee SJ, Jung YH, Oh SY, et al. Vibrio vulnificus VvhA induces NF-kappaB-dependent mitochondrial cell death via lipid raft-mediated ROS production in intestinal epithelial cells. Cell Death Dis, 2015,6: 1655
  103. 103. Vezzulli L, Colwell RR, Pruzzo C. Ocean warming and spread of pathogenic vibrios in the aquatic environment. Microb Ecol, 2013,65(4): 817-825
  104. 104. Waldor MK, Mekalanos JJ. Lysogenic conversion by a filamentous phage encoding cholera toxin. Science, 1996,272(5270): 1910-1914
  105. 105. Castillo D, Kauffman K, Hussain F, et al. Widespread distribution of prophage-encoded virulence factors in marine Vibrio communities. Sci Rep, 2018,8(1): 9973
  106. 106. Fasano A, Baudry B, Pumplin DW, et al. Vibrio cholerae produces a second enterotoxin, which affects intestinal tight junctions. Proc Natl Acad Sci U S A, 1991,88(12): 5242-5246
  107. 107. Di-Pierro M, Lu R, Uzzau S, et al. Zonula occludens toxin structure-function analysis. Identification of the fragment biologically active on tight junctions and of the zonulin receptor binding domain. J Biol Chem, 2001,276(22): 19160-19165
  108. 108. Balebona MC, Morinigo MA, Borrego JJ. Role of extracellular products in the pathogenicity of Vibrio strains on cultured gilt-head seabream (Sparus aurata). Microbiologia, 1995,11(4): 439-446
  109. 109. Balebona MC, Andreu MJ, Bordas MA, et al. Pathogenicity of Vibrio alginolyticus for cultured gilt-head sea bream (Sparus aurata L.). Appl Environ Microbiol, 1998,64(11): 4269-4275
  110. 110. Miyoshi SI, Narukawa H, Tomochika KI, et al. Actions of Vibrio vulnificus metalloprotease on human plasma proteinase-proteinase inhibitor systems: a comparative study of native protease with its derivative modified by polyethylene glycol. Microbiol Immunol, 1995,39(12): 959-966
  111. 111. Bagg A, Neilands J B. Molecular mechanism of regulation of siderophore-mediated iron assimilation. Microbiol Rev, 1987,51(4): 509-518
  112. 112. Braun V, Hantke K, Koster W. Bacterial iron transport: mechanisms, genetics, and regulation. Met Ions Biol Syst, 1998,35: 67-145

Written By

Lixing Huang, Qiancheng Gao, Youyu Zhang, Wei Xu and Qingpi Yan

Submitted: 13 January 2021 Reviewed: 08 February 2021 Published: 11 March 2021