Gill bacteria enable a novel digestive strategy in a wood-feeding mollusk

Abstract

Bacteria play many important roles in animal digestive systems, including the provision of enzymes critical to digestion. Typically, complex communities of bacteria reside in the gut lumen in direct contact with the ingested materials they help to digest. Here, we demonstrate a previously undescribed digestive strategy in the wood-eating marine bivalve Bankia setacea, wherein digestive bacteria are housed in a location remote from the gut. These bivalves, commonly known as shipworms, lack a resident microbiota in the gut compartment where wood is digested but harbor endosymbiotic bacteria within specialized cells in their gills. We show that this comparatively simple bacterial community produces wood-degrading enzymes that are selectively translocated from gill to gut. These enzymes, which include just a small subset of the predicted wood-degrading enzymes encoded in the endosymbiont genomes, accumulate in the gut to the near exclusion of other endosymbiont-made proteins. This strategy of remote enzyme production provides the shipworm with a mechanism to capture liberated sugars from wood without competition from an endogenous gut microbiota. Because only those proteins required for wood digestion are translocated to the gut, this newly described system reveals which of many possible enzymes and enzyme combinations are minimally required for wood degradation. Thus, although it has historically had negative impacts on human welfare, the shipworm digestive process now has the potential to have a positive impact on industries that convert wood and other plant biomass to renewable fuels, fine chemicals, food, feeds, textiles, and paper products.Teredinidae | endosymbionts | symbiosis | xylotrophy | carbohydrate-active enzymes

Biocatalysts for biomass deconstruction from environmental genomics

“…define core microbial communities and enzymatic interactions mediating modular biomass deconstruction. Recently, O'Connor and colleagues used isolate sequencing combined with metagenomics and metaproteomics to identify a novel digestive strategy within the shipworm Bankia setacea [21 ]. In this model, digestive enzymes produced by symbiotic gill bacteria are secreted and transported to the cecum where they are used by the host to deconstruct biomass for nutrition.…”

Secondary metabolism in the gill microbiota of shipworms (Teredinidae) as revealed by comparison of metagenomes and nearly complete symbiont genomes

“…Teredinibacter turnerae strains (with T prefix) were isolated using the method described in Distel el al. 2002 (12), while Bankia setacea symbionts (with Bs prefix) were obtained using the technique indicated in O'Connor et al 2014 (9). Sulfuroxidizing symbionts were isolated using the protocol specified in Altamia et al 2019 (21).…”

“…Shipworm gill symbionts of several different species are thus essential to shipworm nutrition and survival. One of the most remarkable features of the shipworm system is that wood digestion does not take place where the bacteria are located, so that the bacterial cellulase products are transferred from the gill to a nearly sterile cecum (8), where wood digestion occurs (Figure 1) (9). This enables the host shipworms to directly consume glucose and other sugars derived from wood lignocellulose and hemicellulose, rather than the less energetic fermentation products of cellulolytic gut microbes as found in other symbioses.…”

Lignocellulosic biomass: Biosynthesis, degradation, and industrial utilization

“…Interestingly, this wood‐degrading system that rely on the distal production of ligninolytic enzymes is composed of only a small set (namely glycosyl hydrolases from families 5, 6, 9, 10, 11, 45, 53; carbohydrate esterases from families 1, 3, 4, 6, 15, and AA10) of enzymes predicted to be encoded by the endosymbiont genomes. These results are very important to understand the minimal enzymatic requirement to achieve wood degradation .…”