Chapter 13 : Species

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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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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 .

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 .

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.

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.

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.

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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