Microbial Succession of Anaerobic Chitin Degradation in Freshwater Sediments

Abstract

Chitin is massively produced by freshwater plankton species as a structural element of their exoskeleton or cell wall. At the same time, chitin does not accumulate in the predominantly anoxic sediments, underlining its importance as carbon and nitrogen sources for sedimentary microorganisms. We studied chitin degradation in littoral sediment of Lake Constance, Central Europe’s third largest lake. Turnover of the chitin analog methyl-umbelliferyl-N,N-diacetylchitobioside (MUF-DC) was highest in the upper oxic sediment layer, with 5.4 nmol MUF-DC h−1 (g sediment [dry weight])−1. In the underlying anoxic sediment layers, chitin hydrolysis decreased with depth from 1.1 to 0.08 nmol MUF-DC h−1 (g sediment [dry weight])−1. Bacteria involved in chitin degradation were identified by 16S rRNA (gene) amplicon sequencing of anoxic microcosms incubated in the presence of chitin compared to microcosms amended either with N-acetylglucosamine as the monomer of chitin or no substrate. Chitin degradation was driven by a succession of bacteria responding specifically to chitin only. The early phase (0 to 9 days) was dominated by Chitinivibrio spp. (Fibrobacteres). The intermediate phase (9 to 21 days) was characterized by a higher diversity of chitin responders, including, besides Chitinivibrio spp., also members of the phyla Bacteroidetes, Proteobacteria, Spirochaetes, and Chloroflexi. In the late phase (21 to 43 days), the Chitinivibrio populations broke down with a parallel strong increase of Ruminiclostridium spp. (formerly Clostridium cluster III, Firmicutes), which became the dominating chitin responders. Our study provides quantitative insights into anaerobic chitin degradation in lake sediments and linked this to a model of microbial succession associated with this activity.