Features governing symbiont persistence in the squid–vibrio association

Abstract

Experimental studies of the interaction between host and symbiont in a maturing symbiotic organ have presented a challenge for most animal-bacterial associations. Advances in the rearing of the host squid Euprymna scolopes have enabled us to explore the relationship between a defect in symbiont light production and late-stage development (e.g., symbiont persistence and tissue morphogenesis) by experimental colonization with specific strains of the symbiont Vibrio fischeri. During the first four weeks post-inoculation of juvenile squid, the population of wild-type V. fischeri increased 100-fold; in contrast, a strain defective in light production (Δlux) colonized normally the first day, but exhibited an exponential decline to undetectable levels over subsequent weeks. Co-colonization of organs by both strains affected neither the trajectory of colonization by wild type, nor the decline of Δlux levels. Uninfected animals retained the ability to be colonized for at least two weeks post-hatch. However, once colonized by the wild-type strain for 5 days, a subsequent experimentally induced loss of the symbionts could not be followed by a successful recolonization, indicating the host’s entry into a refractory state. However, animals colonized by the Δlux before the loss of their symbionts were receptive to recolonization. Analyses of animals colonized with either a wild-type or a Δlux strain revealed slight, if any, differences in the developmental regression of the ciliated light-organ tissues that facilitate the colonization process. Thus, some other feature(s) of the Δlux strain’s defect also may be responsible for its inability to persist, and its failure to induce a refractory state in the host.

A genomic comparison of 13 symbiotic Vibrio fischeri isolates from the perspective of their host source and colonization behavior

“…Thus, it is possible for an S-type strain to escape the process that selects against it during initiation, perhaps by either (i) becoming established in a crypt before the recruitment of a D-type strain, thereby avoiding competition during the initiation phase, or (ii) existing as a clonal colonization within an individual crypt, thus escaping inter-strain competition. Future studies can resolve between these possibilities by tracking the trajectory of a mixed colonization as the animal matures (Koch et al, 2014), as well as by imaging the fate of mixed populations in each of the organ's six crypts . Whether the selection occurs at the intra-bacterial level, and/or the host is participating by a selective sanctioning (Nyholm et al, 2000;Koch et al, 2014), remains an intriguing and unresolved question.…”

“…In the symbiosis between the squid Euprymna scolopes and the luminous bacterium Vibrio fischeri, as in other environmentally acquired, non-obligatory symbionts, one can experimentally expose an aposymbiotic host to genetically distinct V. fischeri strains, either singly or in combination, and monitor the establishment and dynamics of the resulting symbiont population. By manipulating this highly specific association, one can address fundamental questions concerning the role of strategies like host sanctioning in the evolution of persistent symbiotic associations (Koch et al, 2014).…”

Major evolutionary transitions in individuality

“…Sanction mechanisms seem to be more common in partnerships when symbionts transmit horizontally, where we predict that there will be more conflict to resolve, such as in partnerships with root symbionts, luminous symbionts, and pollinator mutualisms (24,25,48,49).…”

“…For example, legumes provide more resources to more cooperative rhizobia, and squid eliminate symbiotic bacteria that do not luminesce (24,25). Such "sanctions" mechanisms can favor cooperation even when symbiont relatedness is low at the level of the host (Fig.…”

The chemistry of negotiation: Rhythmic, glycan-driven acidification in a symbiotic conversation

“…The symbiont induces postembryonic light-organ development (19), and the organ morphology reaches maturity in 4 wk (20). Host-derived chitin, a polymeric glycan of N-acetylglucosamine, is known to promote the speciesspecific colonization of the squid by V. fischeri (21).…”