The model squid–vibrio symbiosis provides a window into the impact of strain‐ and species‐level differences during the initial stages of symbiont engagement

Abstract

Among horizontally acquired symbioses, the mechanisms underlying microbial strain- and species-level specificity remain poorly understood. Here, confocal-microscopy analyses and genetic manipulation of the squid-vibrio association revealed quantitative differences in a symbiont's capacity to interact with the host during initial engagement. Specifically, dominant strains of Vibrio fischeri, 'D-type', previously named for their dominant, single-strain colonization of the squid's bioluminescent organ, were compared with 'S-type', or 'sharing', strains, which can co-colonize the organ. These D-type strains typically: (i) formed aggregations of 100s-1000s of cells on the light-organ surface, up to 3 orders of magnitude larger than those of S-type strains; (ii) showed dominance in co-aggregation experiments, independent of inoculum size or strain proportion; (iii) perturbed larger areas of the organ's ciliated surface; and, (iv) appeared at the pore of the organ approximately 4×s more quickly than S-type strains. At least in part, genes responsible for biofilm synthesis control the hyperaggregation phenotype of a D-type strain. Other marine vibrios produced relatively small aggregations, while an array of marine Gram-positive and -negative species outside of the Vibrionaceae did not attach to the organ's surface. These studies provide insight into the impact of strain variation on early events leading to establishment of an environmentally acquired symbiosis.

Tracking the cargo of extracellular symbionts into host tissues with correlated electron microscopy and nanoscale secondary ion mass spectrometry imaging

“…We also exposed juvenile squids to strongly 15 N‐enriched nonsymbiotic Vibrionaceae cells, Vibrio campbellii KNH1 and Photobacterium leiognathi KHN6, which are, in comparison with V. fischeri , rare phylotypes in the host's environment (Jones, Maruyama, Ouverney, & Nishiguchi, ). These experiments were done with a 3‐hr exposure to labelled cells, a period when, in the absence of V. fischeri in the environment, these strains exhibit aggregation on the light‐organ surface indistinguishable from that of the nascent symbiont (Koehler et al, ). Under these conditions, these strains produced 15 N‐enrichment patterns in the light organ similar to those induced by V. fischeri cells (Figure and Table S3).…”

“…Strains of four bacteria species were used in this study: wild-type V. fischeri ES114 (Boettcher & Ruby, 1990), V. campbellii KNH1 (formerly, Vibrio parahaemolyticus KNH1; Nyholm, Stabb, Ruby, & McFall-Ngai, 2000), Photobacterium leognathi KNH6 (Koehler et al, 2018), and E. coli RP437 (Zhou, White, Polissi, Georgopoulos, & Raetz, 1998). The Vibrio spp.…”

“…Shortly after hatching, the superficial epithelium sheds mucus in a non‐specific response to environmental peptidoglycan (Nyholm, Deplancke, Gaskins, Apicella, & McFall‐Ngai, ). Some Gram‐negative bacteria, particularly the Vibrionaceae, will attach to the cilia and form aggregates of cells on the organ surface (Koehler et al, ), but eventually, the symbiont shows competitive dominance. In studies with V. fischeri strain ES114, small aggregates of ~5 symbiont cells attach to the host ciliated surface and signal their presence across the ~10,000 cells of the host organ (Altura et al, ; Kremer et al, ).…”

Evolutionary “Experiments” in Symbiosis: The Study of Model Animals Provides Insights into the Mechanisms Underlying the Diversity of Host–Microbe Interactions

“…[45] Comamonas aquatica produces vitamin B12 that affects C. elegans' development and fertility and also breaks down propionic acid to prevent its toxic buildup. [50][51][52] The binary nature of the relationship and well-developed genetics in the bacterial partner, V. fischeri, allow exquisite resolution of the dialogue between partners. Studies using single-species microbes, multimicrobial systems, and humanized worm-microbiome interaction studies reveal metabolic and microbial-microbial interactions relevant in animals with a different body-plan complexity.…”

“…[46] The single-species microbe-host interaction model system is instrumental in understanding the function of specific members of the microbiome. [52] The association is highly specific; in the absence of V. fischeri in the environment of a hatchling, other bacteria do not colonize the organ. Taken together, the use of defined synthetic microbiota ecosystems, guided by the natural history of C. elegans, should help optimize the development of a relevant model system for host-microbiome interaction studies.…”