Cellulose is utilized as a nutritional source by various organisms. It had been long believed that only 21 protozoa, bacteria and fungi, in addition to plants and photo-synthetic bacteria, are abｌe to synthesize cellulases encoded by their own genes. However, the wide spread distribution of cellulases throughout the 23 animal kingdom has been recently recognized. Conventionally, animals digest cellulose by utilizing 24 cellulases derived from symbiotic bacteria in the digestive organs. However, recent molecular biological 25 studies have shown that some cellulase genes are actually encoded on animal chromosomes. In addition, 26 the homologous primary structure of cellulases obtained from various phyla of invertebrates indicates the 27 possible vertical transfer of the cellulase gene from ancient organisms that are now extinct. Studies on 28 cellulase with unique enzymatic properties are expected to be applied to bioethanol production and 29 aquaculture. In the present review, we describe cellulases, with a primary focus on aquatic invertebrates 30 in which both endogenous and exogenous cellulases are involved in the breakdown of cellulose in the 31 digestive organs.

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Recently, numerous species of aquatic invertebrates inhabiting wetlands have been shown to possess endogenous cellulase, following the discovery that termites have cellulase genes encoded in their own genome rather than relying on symbiotic bacteria for decomposing cellulose. Wetlands have been empirically shown to play an important role in the decomposition of land‐originating hard‐to‐degrade polysaccharides such as cellulose. However, the mechanism that connects the cellulase producer and the wetlands remains unknown, which makes it very difficult to evaluate the ecological function of wetlands. Here we found that a macrobenthic bivalve, Corbicula japonica , secretes its cellulase to the wetland sediment. Secreted cellulases are immobilized in the components of the sediment. Moreover, adding cellulose or glucose to C. japonica could trigger its cellulase secretion level. These findings suggest a novel wetland cellulose decomposition mechanism. The decomposition ability of wetlands was previously ascribed only to microbes and/or invertebrates that contain cellulases. Our findings suggest that benthic animals supply wetlands with their enzymes as decomposition agents, while wetland sediments serve as immobilization scaffolds for the enzymes. This system, which was named by us an “environmental bioreactor system,” could provide a key function in wetlands.

Abstract:We investigated the relationship between digestive function and ecological distribution for four related species of Gastropoda (Cerithidea rhizophorarum, Cerithidea cingulata, Batillaria multiformis, and Batillaria attramentaria) inhabiting the Tanaka River estuary (Mie Prefecture, Japan). We compared the digestive enzyme activities for four hard degradable carbohydrates, namely, cellulose, mannan, xylan, and laminarin. Among the investigated four species, Cerithidea rhizophorarum showed the highest cellulase, mannanase, xylanase, and laminarinase activities, and was also dominantly distributed in the estuary reed bed. The results of CN stable isotopic analysis suggested that this species assimilated organic matter derived from reeds. Hard degradable carbohydrates, including plant components derived from the reed bed or from dry land, accumulate in the sediment of estuaries. Estuarine benthic animals are assumed to consume these accumulated hard degradable carbohydrates, as well as microphytobenthos and particulate organic matter (including phytoplankton). Our present findings suggest that Cerithidea rhizophorarum is dominant in reed beds because it can more efficiently digest plant-derived carbohydrates than can Cerithidea cingulata, B. multiformis, and B. attramentaria. To the best of our knowledge, ours is the first study to demonstrate that the specific ecological distribution of related animal species with similar ecological traits can be explained by the efficiency of their digestive enzyme activity.

We investigated inter-species dietary variation and potential cellulose digestion of 12 macroinvertebrate taxa collected from two locations in the estuarine Idoura Lagoon, Sendai Bay. All taxa exhibited cellulase activity (CA), which was higher among surface-deposit feeders (bivalve Macoma contabulata, polychaete Tylorrhynchus osawai, and ocypodid crabs) and obligatory suspension feeders (bivalves Corbicula japonica and Nuttallia japonica) (0.108 to 0.764 µmol min −1 mg-protein −1 ). In contrast, CA was lower among facultative suspension-feeding and deep-deposit feeding polychaetes (Hediste spp. and Heteromastus sp., respectively), and was lowest in the deep-deposit feeding polychaete Notomastus sp. The stable isotope ratios of the macroinvertebrates differed among feeding groups. A δ 13 C-based isotope mixing model revealed that the major dietary component of the surface-deposit feeders was microphytobenthos (34-50%), regardless of their high CAs. Although CAs of obligatory and facultative suspension feeders were comparable to or lower than those of surface-deposit feeders, they were highly dependent on river-derived materials at the station near the freshwater input (38-59%). These results indicate that CA is a common physiological characteristic of macroinvertebrates in estuarine soft-bottom habitats, but the dietary contribution of riverine detritus is not correlated with enzymatic activity. Our findings indicate that several factors affect the realized dietary components of macroinvertebrates, including feeding mode, the selectivity of ingestion, and digestive enzyme activity.