Specific utilization of biopolymers of plant and fungal origin reveals the existence of substrate-specific guilds for bacteria in temperate forest soils

Bacteria play critical roles in soil ecosystems when decomposing structural components of biomass. However, the ability of individual bacterial taxa to utilize various biopolymers is understudied, hampering our understanding of the role of bacteria in the soil carbon cycle. Here, we in situ incubated in forest litter various biopolymers of plant and fungal origin – cellulose, xylan, glucomannan, pectin, lignin, β-1,3-glucan, β-1,3-1,6-glucan, and chitin – to identify bacteria that associated with them during decomposition. After an incubation time of three weeks, all biopolymers were colonized by substantial bacterial numbers. The bacterial communities established on each biopolymer were specific, differing from the community on the surrounding plant litter, which indicates specialization in biopolymer utilization and the existence of distinct substrate-specific guilds. Members of Proteobacteria and Bacteroidetes predominated in all guilds. However, several biopolymers hosted members of other phyla: bacteria affiliated with Planctomycetes were enriched on cellulose, Acidobacteria on xylan, Actinobacteria on pectin, and Firmicutes on glucomannan and β-1,3-1,6-glucan. The communities on lignin had low diversity, were phylogenetically clustered and were mainly composed of Proteobacteria. The communities on chitin showed higher diversity than those on other biopolymers. Approximately 80% of biopolymer-associated bacteria were specialists and were recovered from only one or two biopolymers. Only three specific phylotypes affiliated with Burkholderia, Klebsiella and Hafnia were present on all biopolymers. Bacterial isolation confirmed the involvement of Bacteroidetes in the decomposition of chitin, Firmicutes in the decomposition of glucomannan and β-glucans, and the abundance of decomposers from Proteobacteria on all biopolymers. The proliferation of bacteria was observed on all fungally derived biopolymers and most plant-derived biopolymers. Exceptions were pectin and xylan, where bacterial counts were low – three orders of magnitude lower than in the surrounding plant litter. The results indicate the involvement of distinct, substrate-specific guilds of bacteria in the utilization of biopolymers in forest topsoil. Furthermore, by classifying soil bacteria into substrate-specific guilds, this paper contributes to efforts to assign functional traits of ecological relevance to individual members of the microbial community.