Forever competent: deep‐sea bivalves are colonized by their chemosynthetic symbionts throughout their lifetime

Abstract

SummarySymbiotic bivalves at hydrothermal vents and cold seeps host chemosynthetic bacteria intracellularly in gill cells. In bivalves, the gills grow continuously throughout their lifetime by forming new filaments. We examined how newly developed gill tissues are colonized in bivalves with horizontal and vertical symbiont transmission (Bathymodiolus mussels versus a vesicoymid clam) using fluorescence in situ hybridization and transmission electron microscopy. Symbiont colonization was similar in mussels and clams and was independent of the transmission modes. Symbionts were absent in the growth zones of the gills, indicating that symbionts colonize newly formed gill filaments de novo after they are formed and that gill colonization is a continuous process throughout the host's lifetime. Symbiont abundance and distribution suggested that colonization is shaped by the developmental stage of host cells. Selfinfection, in which new gill cells are colonized by symbionts from ontogenetically older gill tissues, may also play a role. In mussels, symbiont infection led to changes in gill cell structure similar to those described from other epithelial cells infected by intracellular pathogens, such as the loss of microvilli. A better understanding of the factors that affect symbiont colonization of bivalve gills could provide new insights into interactions between intracellular bacteria and epithelial tissues.

Geographical structure of endosymbiotic bacteria hosted by Bathymodiolus mussels at eastern Pacific hydrothermal vents

“…A free-living stage has been identified in vent habitats [42], and the early stages of infection was identified in juvenile mussels [31, 32, 61]. However, it is unknown if the symbiotic stages recycle to the free-living demographic component, as occurs in a siboglinid tubeworm symbiont [62].…”

“…Ambient seawater sampled near adult mussels contained lower densities (~1.74 × 10 5 /l) that declined with distances from the Bathymodiolus patch. Once settling mussel larvae are infected, rapid proliferation of the bacteria would greatly enrich the abundance of a small number founding strains (e.g., [31, 32]). Bathymodiolus adults from the Mid-Atlantic Ridge were estimated to host ~2.5 × 10 12 symbionts per individual [61]; thus, the high variance among host individuals probably reflects initial sampling bias associated with infections and secondary biases that accrue during enrichment.…”

“…Initial infections of larvae occur in a range of epithelial tissues and then shift to the developing gills, where the bacteria proliferate [30–32]. Researchers hypothesized that dispersing mussel larvae might carry hitchiking symbionts from natal sites to new habitats in which they settle [8], but the genetic evidence was insufficient and inconclusive.…”

Niche-Specific Impact of a Symbiotic Function on the Persistence of Microbial Symbionts within a Natural Host

“…Patterns of assembly of microbial consortia have been similarly linked to host development for the human gut microbiome, with massive alterations in composition correlating well with developmental transitions in eating behaviors (33). Finally, in bivalves at hydrothermal vents, the developmental stage of gill tissue is a factor that contributes to colonization by chemosynthetic symbionts (34).…”

Identification and gene expression of multiple peptidoglycan recognition proteins (PGRPs) in the deep-sea mussel Bathymodiolus azoricus , involvement in symbiosis?

“…Nevertheless, gill colonisation by endosymbiotic bacteria seems to be a continuous process throughout mussels lifetime (Wentrup et al, 2014), suggesting a necessity for the host to produce constantly a signal of cooperation to indicate the correct location for the colonisation of future symbionts as it has been suggest in the association between the weevil Sitophilus zeamais and its symbionts (Reynolds and Rolff, 2008). Therefore we may postulate that (ii) Ba-PGRP 3 and 5 would rather be used as a signal of cooperation in natural population to acquire constantly new symbionts.…”