TY - JOUR

T1 - How It All Begins

T2 - Bacterial Factors Mediating the Colonization of Invertebrate Hosts by Beneficial Symbionts

AU - Ganesan, Ramya

AU - Ec, Max

AU - Kaltenpoth, Martin

AU - Flórez, Laura V.

PY - 2023

Y1 - 2023

N2 - 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.

AB - 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.

U2 - 10.1128/mmbr.00126-21

DO - 10.1128/mmbr.00126-21

M3 - Review

C2 - 36301103

VL - 86

JO - Microbiology and Molecular Biology Reviews

JF - Microbiology and Molecular Biology Reviews

SN - 1092-2172

IS - 4

M1 - e0012621

ER -