Establishment of an animal–bacterial association: Recruiting symbiotic vibrios from the environment

Abstract

While most animal-bacterial symbioses are reestablished each successive generation, the mechanisms by which the host and its potential microbial partners ensure tissue colonization remain largely undescribed. We used the model association between the squid Euprymna scolopes and Vibrio fischeri to examine this process. This light organ symbiosis is initiated when V. fischeri cells present in the surrounding seawater enter pores on the surface of the nascent organ and colonize deep epithelia-lined crypts. We discovered that when newly hatched squid were experimentally exposed to natural seawater, the animals responded by secreting a viscous material from the pores of the organ. Animals maintained in filtered seawater produced no secretions unless Gram-negative bacteria, either living or dead, were reintroduced. The viscous material bound only lectins that are specific for either N-acetylneuraminic acid or N-acetylgalactosamine, suggesting that it was composed of a mucus-containing matrix. Complex ciliated fields on the surface of the organ produced water currents that focused the matrix into a mass that was tethered to, and suspended above, the light organ pores. When V. fischeri cells were introduced into the seawater surrounding the squid, the bacteria were drawn into its fluid-filled body cavity during ventilation and were captured in the matrix. After residing as an aggregate for several hours, the symbionts migrated into the pores and colonized the crypt epithelia. This mode of infection may be an example of a widespread strategy by which aquatic hosts increase the likelihood of successful colonization by rarely encountered symbionts.

‘Candidatus Streptomyces philanthi’, an endosymbiotic streptomycete in the antennae of Philanthus digger wasps

“…Alternatively, the bacteria may be taken up from the environment with certain mechanisms preventing the uptake of non-symbiotic bacteria, a transmission route that has been demonstrated for the symbionts of the squid Euprymna scolopes (McFallNgai & Ruby, 1991;Nishiguchi, 2002;Nyholm et al, 2000;Nyholm & McFall-Ngai, 2004). The following evidence points to vertical transmission of the bacteria from mother to offspring in Philanthus: (i) the bacteria are secreted into the brood cell and later taken up by the larva and (ii) a female larva that was reared in the absence of the white substance in its brood cell apparently lacked the symbiotic bacteria as an adult (Kaltenpoth et al, 2005).…”

Exploring host–microbiota interactions in animal models and humans

“…Within 1-2 h of hatching, peptidoglycan from environmental microbes trigger secretion of mucus outside the light organ (Nyholm et al 2002). This mucus further aggregates Gram-negative bacteria outside the light organ, which, within a few hours, becomes dominated by V. fischeri (Nyholm et al 2000;Nyholm and McFall-Ngai 2003). By 4-6 h after the squid hatch, V. fischeri begin to migrate into the pores of the light organ through the epitheliallined ducts and settle into the deep crypts (McFall-Ngai and Ruby 1998;Nyholm et al 2000).…”

“…This mucus further aggregates Gram-negative bacteria outside the light organ, which, within a few hours, becomes dominated by V. fischeri (Nyholm et al 2000;Nyholm and McFall-Ngai 2003). By 4-6 h after the squid hatch, V. fischeri begin to migrate into the pores of the light organ through the epitheliallined ducts and settle into the deep crypts (McFall-Ngai and Ruby 1998;Nyholm et al 2000). Once inside the light organ, V. fischeri ''signal'' their presence to the host by release of lipopolysaccharide (LPS) and peptidoglycan, classic examples of microbial-associated molecular patterns Koropatnick et al 2004).…”

Selective recruitment of bacteria during embryogenesis of an earthworm

“…In the squid-Vibrio association, the juvenile nascent light organ creates a current to draw bacteria from the seawater. Vibrio fischeri are selectively collected from the mixed bacterial population in the sea water and accumulate by binding specifically to the mucus of the symbiotic organ with a few contaminant cells (Nyholm et al, 2000;Nyholm and McFall-Ngai, 2003). After a waiting period (2-3 h), V. fischeri migrate into the nascent light organ through ciliated ducts that possess an oxidatively stressful environment to exclude other bacterial types (Small and McFall-Ngai, 1999;Davidson et al, 2004).…”