Achieving a multi-strain symbiosis: strain behavior and infection dynamics

Abstract

Strain diversity, while now recognized as a key driver underlying partner dynamics in symbioses, is usually difficult to experimentally manipulate and image in hosts with complex microbiota. To address this problem, we have used the luminous marine bacterium Vibrio fischeri, which establishes a symbiosis within the crypts of the nascent light organ of the squid Euprymna scolopes. Competition assays in newly hatched juvenile squid have shown that symbiotic V. fischeri are either niche-sharing "S strains", which share the light organ when co-inoculated with other S strains, or niche-dominant "D strains", which are typically found alone in the light organ after a co-colonization. To understand this D strain advantage, we determined the minimum time that different V. fischeri strains needed to initiate colonization and used confocal microscopy to localize the symbionts along their infection track. Further, we determined whether symbiont-induced host morphogenic events also occurred earlier during a D strain colonization. We conclude that D strains colonized more quickly than S strains. Nevertheless, light-organ populations in field-caught adult squid often contain both D and S strains. We determined experimentally that this symbiont population heterogeneity might be achieved in nature by a serial encounter of different strains in the environment.

HbtR, a heterofunctional homolog of the virulence regulator TcpP, facilitates the transition between symbiotic and planktonic lifestyles inVibrio fischeri

“…Based on work presented here, including a demonstration that MCP genes repressed by LitR are involved in light-organ colonization (Fig. 2), we posit that the litR- mutant colonization benefit (4) may have been a priority effect (38), resulting from the increase in both motility and chemotaxis into the light organ by that mutant. We hypothesize that the lower level of colonization observed for the litR mutant in single-strain experiments (31) may have been due to dysregulation of a separate symbiotic process, perhaps extracellular polysaccharide production.…”

“…Juvenile squid colonization experiments were performed as described previously (38), with juvenile squid exposed to V. fischeri strains at 1,000– 6,000 CFU/mL either for 3 h or overnight, as indicated, before being placed in fresh sterile seawater until euthanizing by freezing. Colonization competition experiments were performed by exposing juvenile squid to a 1:1 inoculum of each strain.…”

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.…”

“…The E. scolopes light organ symbiosis offers a rich set of opportunities to study many aspects of symbiosis, from ecology and evolutionary biology to the molecular mechanisms underlying establishment and maintenance of a symbiotic association. [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. [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.…”

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

“…To reach the crypts, the symbiont cells migrate into a pore and through a ciliated duct and antechamber, which are separated from a crypt by a narrow bottleneck (Sycuro et al, ). Regardless of the aggregation size and how many V. fischeri cells migrate into host the ducts and antechambers, on average, only a single V. fischeri cell successfully grows out to populate each of the six crypts (Figure c; Bongrand & Ruby, ; Wollenberg & Ruby, ). Within the crypts, the symbiont cells interface with a microvillous epithelium.…”