Extracellular digestion in two co-occurring intertidal mussels ( Perna perna (L.) and Choromytilus meridionalis (Kr)) and the role of enteric bacteria in their digestive ecology

Abstract

The style enzymes and enteric bacteria of two intertidal mussels, Perna perna (L.) and Choromytilus meridionalis (Kr), were tested for activity on ten structural and storage carbohydrates. Both mussels digested the storage carboyhydrates amylose, glycogen and laminarin, and the structural carbohydrate carboxymethyl cellulose (CMC). C. meridionalis broke down the digested storage carbohydrates with equal efficiency, while P. perna digested laminarin and glycogen more efficiently than amylose. P. perna produced large volumes of enzymes with low dissociation rates, while the opposite was true for C. meridionalis. As a result, P. perna released significantly more glucose (ANOVA: P<0.05) from all substrates, even though it had significantly lower specific enzyme activities ( P<0.05). Likewise, both mussels could digest bacteria isolated from their guts, but P. perna digested more bacterial strains, more efficiently, than C. meridionalis. In contrast, C. meridionalis housed larger populations of gut bacteria which digested carbohydrates more efficiently than those from P. perna. Mixed bacterial cultures from both mussels showed consistently high activity on storage carbohydrates. Activity was consistent, but low, on two structural carbohydrates (CMC and mannan) but sporadic on the other structural compounds (carrageenin, fucoidan and xylan). Electron microscopy showed that both mussels housed two distinct populations of bacteria: resident spirochaete bacteria (presumably Cristispira spp) in the style, and a mixture of rod, coccoid and filamentous bacteria associated with the gut contents. The sporadic presence of bacteria which digest most structural carbohydrates, and their association with the gut contents, indicate that these bacteria are transient. This means that the association between the mussels and their enteric bacteria is incidental rather than obligatory. The spirochaete bacteria in the style have an obligate relationship with the mussels and may increase the amount of carbohydrases produced, but not the range of enzymes available to the host.