An out-of-body experience: the extracellular dimension for the transmission of mutualistic bacteria in insects

Symbiotic partnerships with beneficial microbes drive many metabolic and defensive adaptations in animals and plants. While intracellular symbionts often show genome erosion and co-evolution with their hosts, the consequences of extracellular lifestyles are less understood despite being widespread and functionally important. Using insect-bacteria symbioses as a model, this review highlights diverse routes of extracellular symbiont transfer, unified by the bacteria's ability to survive outside hosts, imposing different genomic, metabolic, and morphological constraints. The evolutionary implications of transmission routes (intracellular versus extracellular) do not necessarily match those of transmission mode (vertical versus horizontal), a key distinction for understanding genomic and physiological outcomes for both partners.

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Abstract

Across animals and plants, numerous metabolic and defensive adaptations are a direct consequence of symbiotic associations with beneficial microbes. Explaining how these partnerships are maintained through evolutionary time remains one of the central challenges within the field of symbiosis research. While genome erosion and co-cladogenesis with the host are well-established features of symbionts exhibiting intracellular localization and transmission, the ecological and evolutionary consequences of an extracellular lifestyle have received little attention, despite a demonstrated prevalence and functional importance across many host taxa. Using insect-bacteria symbioses as a model, we highlight the diverse routes of extracellular symbiont transfer. Extracellular transmission routes are unified by the common ability of the bacterial partners to survive outside their hosts, thereby imposing different genomic, metabolic and morphological constraints than would be expected from a strictly intracellular lifestyle. We emphasize that the evolutionary implications of symbiont transmission routes (intracellular versus extracellular) do not necessarily correspond to those of the transmission mode (vertical versus horizontal), a distinction of vital significance when addressing the genomic and physiological consequences for both host and symbiont.