How It All Begins: Bacterial Factors Mediating the Colonization of Invertebrate Hosts by Beneficial Symbionts

Abstract

Beneficial associations with bacteria are widespread across animals, spanning a range of symbiont localizations, transmission routes, and functions. While some of these associations have evolved into obligate relationships with permanent symbiont localization within the host, the majority require colonization of every host generation from the environment or via maternal provisions. Across the broad diversity of host species and tissue types that beneficial bacteria can colonize, there are some highly specialized strategies for establishment yet also some common patterns in the molecular basis of colonization. This review focuses on the mechanisms underlying the early stage of beneficial bacterium-invertebrate associations, from initial contact to the establishment of the symbionts in a specific location of the host's body. We first reflect on general selective pressures that can drive the transition from a free-living to a host-associated lifestyle in bacteria. We then cover bacterial molecular factors for colonization in symbioses from both model and nonmodel invertebrate systems where these have been studied, including terrestrial and aquatic host taxa. Finally, we discuss how interactions between multiple colonizing bacteria and priority effects can influence colonization. Taking the bacterial perspective, we emphasize the importance of developing new experimentally tractable systems to derive general insights into the ecological factors and molecular adaptations underlying the origin and establishment of beneficial symbioses in animals.

Keywords: animal-microbe interactions; beneficial bacteria; host colonization; molecular factors; symbiosis.

FIG 1

Overview of known bacterial molecular mechanisms used for colonization of animal hosts in symbioses that require reentry of the symbionts into the host tissues every generation from the parents or the environment. The mechanisms addressed in the review are depicted on the left and invertebrate-bacterium symbioses described in the review are depicted on the right. The colored dots below the figures of the hosts indicate the mechanisms that their respective symbionts are known to use during colonization (color legend shown in the middle) The symbiotic systems include hosts living in marine, terrestrial, and freshwater habitats, as follows: bobtail squids (A), giant tubeworms (B), sponges (C), broad-headed bean bugs (D), tsetse flies (E), fruit flies (F), honey bees (G), entomopathogenic nematodes (H), and leeches (I). RNS, reactive nitrogen species; PGRPs, peptidoglycan recognition proteins; TxSS, any type secretion system.

FIG 2

Localization of beneficial symbionts in the following invertebrate systems discussed in the review: bobtail squids (based on reference 105) (A), giant tubeworms (based on reference 264) (B), sponges (based on references and 266) (C), broad-headed bean bugs (based on reference 267) (D), tsetse flies (based on reference and 269) (E), fruit flies (based on reference 270) (F), honey bees (based on reference 271) (G), entomopathogenic nematodes (based on reference 152) (H), and leeches (based on reference 272) (I). Red highlights indicate the specific location of a symbiont in an organ/body of the host. Multiple symbiotic strains or species may sometimes colocalize together, which is indicated in darker red.