Shift from widespread symbiont infection of host tissues to specific colonization of gills in juvenile deep-sea mussels.
Among endosymbioses it is unusual for the symbiotic bacteria to colonize much more of the animal then just a specialized organ, with the exception of hosts that pass on symbionts vertically through specialized gonadal cells. Within Bathymodilus mussels, a genus that is found throughout the ocean at both hydrothermal vents and cold seeps, symbionts are thought to be acquired horizontally, although it is unclear at which stage this occurs as mussels as small as 0.12mm have been shown to harbour symbionts.
In adult and late juvenile Bathymodilus methane and sulfur oxidizing bacteria are constrained to specialized bacteriocytes in the gill tissue. This is the site where all the required nutrients are available and the large surface area to volume ratio and exposure to seawater ensure maximum efficiency of nutrient transfer both to symbiont and host (adjacent to haemolymph lacuna). Unusually though, early juvenile stages have been shown to harbour symbionts within epithelial cells of other tissues. To discover which tissues and whether or not these were exclusively symbiotic bacteria Wentrup, et al.,(2013) used fluorescence in situ hybridization (FISH) with probes specific to the symbiont groups as well as a general eubacterial probe on mussels at different stages of development (4-21mm).
In all mussels they found both types of symbiont within bacteriocytes in the gill tissue. In the smaller individuals (4-7mm) there was evidence of both symbiotic bacteria in epithelial cells of the mantle, foot and retractor mussel (see fig. 1). In all individuals looked at there were no other bacteria found within host cells, indicating that there must be a mechanism for selecting only the beneficial bacteria. In all individuals larger then 7mm endosymbionts were exclusively in the gills.
It is interesting to think that these bivalves ‘allow’ indiscriminate colonization of epithelia at early stages in development. It might be that the earlier stages require more energy from the symbiosis so allow colonization of other cells although it has been postulated that filtration feeding, that does still occur, would make up for any small amount of nutrients provided by these non gill symbionts. However the gill in many bivalves generally develops later then the mantle and foot so this theory does seem plausible. There may be some genetic mechanism, turned on at a specific stage in ontogeny that has a microbicidal effect in all tissues apart from the gill, perhaps a digestive enzyme. It may also be that the bacteria just cannot survive once the tissues have outgrown them, with diffusion distances increasing they may dwindle due to nutrient deprivation.
Assuming that transmission is horizontal (same study could be performed on spawning individuals to determine if symbionts occur in the gonads) there must be a recognition mechanism that distinguishes the two symbiont groups from other potentially pathogenic bacteria and possibly initiates phagocytosis into specialized bacteriocytes though little is known about how this takes place. Bivalve immunity is carried out by haemocytes that engulf bacteria as well as producing microbicidal agents. At some point in the history of this symbiosis the haemocytes lost their ability to destroy these symbiotic bacteria and allowed them to enter the tissue of the animal. Perhaps the early (in ontogeny) immune system of these mussels is not developed enough to prevent bacterial contamination of other organs, though I am inclined to think that it has benefit to the developing mollusk. The problem with studying these kind of symbioses is the difficulty of sampling. in this study only 13 mussels were actually used so extrapolation of data to whole populations is risky.
Figure 1. FISH signals for sulfur oxidizing symbionts (green) and methane oxidizing symbionts (red) in the mantle and gill of juvenile mussels. Adapted from (Wentrup, et al., 2013).
Wentrup, C., Wendeberg, A., Huang, J. Y., Borowski, C., & Dubilier, N. (2013). Shift from widespread symbiont infection of host tissues to specific colonization of gills in juvenile deep-sea mussels. The ISME journal, 7(6), 1244–7.