Chapter 9 : Experimental Models of Symbiotic Host-Microbial Relationships: Understanding the Underpinnings of Beneficence and the Origins of Pathogenesis

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The study of beneficial associations of plants and animals with microorganisms is in its infancy. This chapter describes the very beginnings of a characterization. The understandable historical focus on determining the basis of devastating pathogenic diseases, as well as technical impediments to studying the dynamic and complex interactions between microbial communities and their hosts, have hindered one's ability to obtain an accurate understanding of the relationships of animals and plants with the microbial world. Studies of mutants in rhizobia indicate that components of the symbiont’s lipopolysaccharide (LPS) are also important in inducing normal infection thread formation and the eventual release of the symbionts into host cortical cells. Overall, a remarkable number of host mechanisms used to avoid infection by pathogenic microbes, such as production of reactive oxygen species (ROS) and “antimicrobial” proteins and peptides, appear to play significant roles in the legume-rhizobium (LR) and squid-vibrio (SV) associations. Taken together, the available data on the LR and SV symbioses suggest that interactions between the partners involve molecules traditionally associated with host defense, although they appear to be modulated differently in these beneficial associations. Studies of the coevolution and coadaptation of humans and their microbial communities present an opportunity to gain new understanding about how our ancient migrations, dietary changes, and social innovations helped shaped our current biology, and how they influenced the origins of, our susceptibilities to, and the spread of various pathogenic symbioses.

Citation: McFall-Ngai M, Gordon J. 2006. Experimental Models of Symbiotic Host-Microbial Relationships: Understanding the Underpinnings of Beneficence and the Origins of Pathogenesis, p 147-166. In Seifert H, DiRita V (ed), Evolution of Microbial Pathogens. ASM Press, Washington, DC. doi: 10.1128/9781555815622.ch9

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Type III Secretion System
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Symbiont-induced development of the host tissues in the squid-vibrio association. (Upper left) Diagram of a ventral dissection of a newly hatched , revealing the position of the light organ in the animal’s body cavity (dashed line to an expanded view of the organ). (Upper half, light organ surface) Each complex ciliated field on the lateral surface of the organ is composed of an anterior appendage (aa) and a posterior appendage (pa), which are single layers of epithelial cells overlying a blood sinus (bs). At the base of these appendages is a ciliated field that surrounds the three pores (p) where the symbionts will enter host tissues. This ciliated epithelium serves two functions: the beat of the cilia entrains environmental bacteria into the vicinity of the pores, and the cells of the field secrete mucus in which symbionts will be harvested. Both nonspecific environmental bacteria and bacterial symbionts induce a series of dramatic alterations in this superficial ciliated epithelium in the hours to days following hatching of the host from the egg. First ( ), interactions with nonspecific environmental bacteria and their associated peptidoglycan induce mucus shedding from the ciliated epithelium. Gram-negative bacteria begin to aggregate in this mucus and, concomitantly, macrophagelike hemocytes traffic into the blood sinuses underlying the superficial epithelium. In a second phase ( ), symbiont cells () become numerically dominant in the mucus. They then enter pores on the organ surface (arrow) and travel down ducts (d) into crypts (c), where the symbiont population grows to fill to the crypt spaces. Hemocyte number continues to increase in the blood sinuses, and the first signs of apoptosis in the ciliated epithelium occur around the time that the aggregated symbionts are in the ducts of the organ. Once inside the crypt spaces ( ), cells induce regression of the superficial ciliated epithelium of the light organ, which is remote from the population of colonizing symbionts. By 12 hours, a large proportion of the epithelial cells are undergoing apoptosis, and the blood sinus is filled with hemocytes. Upon continued colonization of the crypts with symbionts ( ), further mucus production and harvesting of symbionts ceases, although this behavior can be restored by antibiotic-curing the light organ of its symbionts. By 4 to 5 days following colonization ( ), the ciliated epithelium of the light organ has been completely lost. The lipopolysaccharide (LPS) and peptidoglycan (PGN) of the symbiont act synergistically to induce the complete regression of these ciliated fields. (Lower half, light organ interior) In response to interactions with the symbionts, the ducts constrict, a behavior that can be mimicked by exposure to PGN alone. The crypt cells exhibit a dramatic increase in the density of the microvilli. In addition, they show a fourfold increase in volume in response to interactions with the symbiont. mutants defective in light production do not induce cell swelling and are incapable of maintaining a persistent normal symbiosis.

Citation: McFall-Ngai M, Gordon J. 2006. Experimental Models of Symbiotic Host-Microbial Relationships: Understanding the Underpinnings of Beneficence and the Origins of Pathogenesis, p 147-166. In Seifert H, DiRita V (ed), Evolution of Microbial Pathogens. ASM Press, Washington, DC. doi: 10.1128/9781555815622.ch9
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Composite of characters shared between mutualistic and pathogenic symbiotic associations. In both types of associations, the bacterial partners may have genomic elements that are involved in the dynamics of the symbiosis, including plasmids (sym), phages (ph), genomic (pathogenicity) islands (gi), transposons (tp), and mobilization loci (mob). In addition, the induction of similar, if not homologous, mechanisms for sensing and responding to the environment have been reported, including two-component regulatory systems (tcr), iron acquisition (Fe), and specific outer membrane proteins (omp), and autoinducers (ai) that enable the bacteria to sense and respond to being at high population density. The bacterial partner may interact directly with the host cells through conserved bacterial surface molecules such as lipopolysaccharide (LPS) and peptidoglycan (PGN), and/or through more specific exopolysaccharides (EPS), a type III secretion system (tss), lectins (le), or fimbriae (fim). Studies thus far on host cells demonstrate shared responses to mutualistic or pathogenic associations. In a number of cases, various bacterial ligands have been shown to interact with receptor proteins on host cell surfaces that include an extracellular leucine-rich repeat domain (LRR), a transmembrane domain (tm), and a kinase domain (kd). Circumstantial evidence exists that signal transduction pathways similar to the NF-КB and JAK/STAT pathways, which mediate responses to pathogens, are also present in beneficial associations. Reactive oxygen species, including nitric oxide (NO), hydrogen peroxide (HO), and hypohalous acid (HOCl), are host molecules also involved in the communication between host and symbiont in both beneficial and pathogenic associations.

Citation: McFall-Ngai M, Gordon J. 2006. Experimental Models of Symbiotic Host-Microbial Relationships: Understanding the Underpinnings of Beneficence and the Origins of Pathogenesis, p 147-166. In Seifert H, DiRita V (ed), Evolution of Microbial Pathogens. ASM Press, Washington, DC. doi: 10.1128/9781555815622.ch9
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The types of symbioses based on the effect of the association on the fitness of the partners

Citation: McFall-Ngai M, Gordon J. 2006. Experimental Models of Symbiotic Host-Microbial Relationships: Understanding the Underpinnings of Beneficence and the Origins of Pathogenesis, p 147-166. In Seifert H, DiRita V (ed), Evolution of Microbial Pathogens. ASM Press, Washington, DC. doi: 10.1128/9781555815622.ch9

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