Digestive environments of benthic macroinvertebrate guts: Enzymes, surfactants and dissolved organic matter

Abstract

Hydrolytic enzyme activity, surfactancy, and dissolved organic matter in the digestive lumens of 19 benthic echinoderm and polychaete species were examined, using consistent and quantifiable methods. Enzyme activities were compared with those of extracellular enzymes from ambient sediments. Enzyme activities ranged over five orders of magnitude, with averages decreasing in the order polychaetes > echinoderms > sediment. Highest activities in animals were usually associated with the fluid phase in midgut sections, with posteriorward decreases indicating little export to the external environment. At some phyletic levels, activity correlated inversely with animal size. Hydrolase patterns reflected food type; for example, high 1ipase:protease ratios in carnivores reflected esterified lipids in their diets. High surfactant activity was found in gut sections having high enzyme activity. Deposit feeders had the most intense surfactancy, including evidence for micelles. While enzymes reflected the biochemical nature of the digestible food substrate regardless of feeding mode (e.g., deposit vs. suspension feeder), surfactants reflected dilution of this digestible substrate with mineral grains. Dissolved organic matter levels were high, with amino acids reaching levels > 1 M and lipids commonly 1 g L-r. Among polychaete deposit-feeders, low molecular weight amino acids reflected the composition of the food substrate, but were present at much higher concentrations than could be explained by sediment present in the gut-suggesting longer residence times for fluid than for transiting sediment particles. Deposit feeder digestive fluids are better able to solubilize sedimentary food substrates than are sedimentary extracellular enzymes, owing to either more powerful solubilizing agents or to their deployment in freely diffusing, dissolved form. Gut environments may lead to chemical condensation as well as solubilization reactions.

Gut-associated microbial symbionts of the marsh fiddler crab, Uca pugnax

“…The observed decline in hindgut activity, compared with the other gut sections, has been reported in other invertebrate detritivores (Mayer et al 1997). In order to reduce enzyme loss to the environment, the host may reabsorb enzymes in the posterior midgut and/or may control fluid transport along the gut (Jumars 1993).…”

“…Sample preparation and enzyme activity measurement followed procedures in Mayer et al (1997) with the following modifications. Crab stomach, hepatopancreas, midgut and hindgut sections were removed with sterile dissecting tools.…”

“…The fluorophores used, methylumbelliferone (MUF) and methylcoumarinyl amide (MCA), can be detected at low levels, have a wide range of detection and have been shown to be a reliable method of measuring extracellular enzymatic activity in many environments, including within the guts of deposit feeders (Mayer 1989;Mayer et al 1997). These synthetic substrates are relatively non-fluorescent, whereas the hydrolytic products Reader 4000 (PerSeptive Biosystems).…”

“…All enzymes produced by decapod crustaceans are thought to be generated here and passed into the stomach and midgut lumen (Brunet et al 1994;. The majority of active enzymes are expected to be retained within the stomach and midgut, possibly via gut fluid reflux (Jumars 1993;Mayer et al 1997). Yet some host-derived enzymes are likely passed with gut contents into the hindgut.…”

Micro-trace fossils reveal pervasive reworking of Pliocene sapropels by low-oxygen-adapted benthic meiofauna

“…Benthic animals facilitate sediment irrigation and oxygen ingress through burrowing [1][2][3] and accelerate organic matter (OM) degradation through ingestion, physical comminution and enzymatic breakdown 1,5,6 . Since their proliferation in the Cambrian, animal burrowers have left an indelible signature on the sedimentary record in almost all marine environments 7 , with the seeming exception being low-oxygen environments that are typified by laminated sediments lacking visible evidence of animal activity 8 .…”