Cultivation and Fluorescent in situ hybridization suggest that some shipworm species acquire endosymbiotic bacteria through indirect horizontal transmission

Abstract

ABSTRACTBeneficial microbial symbionts provide essential functions for their host from nutrients to defense against disease. Whether hosts acquire their symbionts directly from parents (vertical transmission) or by sampling from the environment (horizontal transmission) can have dramatic impacts on host adaptability and, in the case of ecosystem engineers, ecosystem health. Wood-boring bivalve mollusks (Teredinidae shipworms) act as ecosystem engineers in marine environments, creating habitat out of submerged wood for fish and invertebrates. Essential to shipworm success is their community of endosymbiotic gill bacteria that produce the enzymes necessary for wood digestion. How shipworms acquire their symbionts, however, remains largely unexplored. Using culturing, fluorescencein-situhybridization, confocal microscopy, and tank experiments, we provide evidence suggesting the mode of symbiont transmission the shipworms for either the shipworm,Lyrodus pedicellatusorTeredo bartschior both. Symbiotic bacteria were not detected by cultivation or microscopy in brooding larvae within gravid adults or as veliger larvae collected from the water column, but were observed in adult specimens and juveniles that had begun burrowing into wood. These data suggest that the specimens examined have both aposymbiotic and symbiotic life phases and acquire their symbionts through indirect horizontal transmission. Our findings reveal how the long-term broodersL. pedicellatusand/orT. bartschiacquire their gill endosymbionts.IMPORTANCEHow eukaryotic hosts acquire their microbial symbionts can have significant consequences for their ability to adapt to varied environments. Although wood-boring bivalve shipworms have diverse reproductive strategies and are found in unique environments across the globe, little is known about how they transmit their essential gill endosymbionts. We used the closely related shipworms,Lyrodus pedicellatusand/orTeredo bartschito study how these long-term brooding shipworms acquire their gill endosymbionts. Our work, unlike previous claims for the broadcast spawning speciesBankia setacaewhich reportedly transmits its symbionts directly from parent to offspring, suggests that juvenileL. pedicellatusand/orT. bartschiacquire their symbionts through horizontal transmission rather than directly from their parents. This work reveals the mechanism by which some brooding shipworm species acquire their symbionts, adding to our limited understanding of intracellular symbiont transmission of Teredinidae.