Identification of microbial populations driving biopolymer degradation in acidic peatlands by metatranscriptomic analysis

Abstract

Northern peatlands play a crucial role in the global carbon balance, serving as a persistent sink for atmospheric CO2 and a global carbon store. Their most extensive type, Sphagnum-dominated acidic peatlands, is inhabited by microorganisms with poorly understood degradation capabilities. Here, we applied a combination of barcoded pyrosequencing of SSU rRNA genes and Illumina RNA-Seq of total RNA (metatranscriptomics) to identify microbial populations and enzymes involved in degrading the major components of Sphagnum-derived litter and exoskeletons of peat-inhabiting arthropods: cellulose, xylan, pectin and chitin. Biopolymer addition to peat induced a threefold to fivefold increase in bacterial cell numbers. Functional community profiles of assembled mRNA differed between experimental treatments. In particular, pectin and xylan triggered increased transcript abundance of genes involved in energy metabolism and central carbon metabolism, such as glycolysis and TCA cycle. Concurrently, the substrate-induced activity of bacteria on these two biopolymers stimulated grazing of peat-inhabiting protozoa. Alveolata (ciliates) was the most responsive protozoa group as confirmed by analysis of both SSU rRNA genes and SSU rRNA. A stimulation of alphaproteobacterial methanotrophs on pectin was consistently shown by rRNA and mRNA data. Most likely, their significant enrichment was due to the utilization of methanol released during the degradation of pectin. Analysis of SSU rRNA and total mRNA revealed a specific response of Acidobacteria and Actinobacteria to chitin and pectin, respectively. Relatives of Telmatobacter bradus were most responsive among the Acidobacteria, while the actinobacterial response was primarily affiliated with Frankiales and Propionibacteriales. The expression of a wide repertoire of carbohydrate-active enzymes (CAZymes) corresponded well to the detection of a highly diverse peat-inhabiting microbial community, which is dominated by yet uncultivated bacteria.

Genome Analysis of Fimbriiglobus ruber SP5T, a Planctomycete with Confirmed Chitinolytic Capability

“…This study began with attempts to detect the substrate-induced response of F. ruber-like planctomycetes to amendment of Sphagnum-derived peat from the peat bog Obukhovskoye with chitin. For this purpose, we reanalyzed the small subunit (SSU) rRNA data set retrieved in our recent metatranscriptomic study (19), which assessed the substrate-induced response of peat-inhabiting microorganisms to amendments with various key biopolymers, including cellulose, xylan, pectin, and chitin. The 16S rRNA reads from F. ruber-like planctomycetes were sorted out using a species-level identity threshold of 97% from the sequence sets corresponding to four experimental incubations with different biopolymers and the control incubation without added substrate.…”

“…Recent molecular study of microbial degradation of chitin in an agricultural soil suggested involvement of Singulisphaera-like planctomycetes in this process (18). Additional evidence for the existence of chitinolytic planctomycetes was obtained in a metatranscriptome-based study of microbial populations driving biopolymer degradation in acidic peatlands (19). Although no changes in the relative abundance of planctomycetes within the whole bacterial community were observed in response to the amendment with chitin, some groups within uncultivated planctomycetes, in particular Gemmata-like bacteria, were clearly stimulated by the availability of this biopolymer.…”

“…Recently, we described one novel member of the family Gemmataceae from acidic peat bogs, namely, Fimbriiglobus ruber SP5 T (20). This planctomycete was isolated from the peat bog Obukhovskoye, which served as a source of peat material used in the metatranscriptomic study of Ivanova et al (19). Although strain SP5 T was unable to degrade chitin from crab shells, weak growth was observed on amorphous chitin prepared as described elsewhere (21).…”

Comparative Genomics of Four Isosphaeraceae Planctomycetes: A Common Pool of Plasmids and Glycoside Hydrolase Genes Shared by Paludisphaera borealis PX4T, Isosphaera pallida IS1BT, Singulisphaera acidiphila DSM 18658T, and Strain SH-PL62

“…As revealed by molecular surveys, these bacteria are common inhabitants of boreal Sphagnum -dominated peatlands (Dedysh, 2011; Ivanova and Dedysh, 2012; Serkebaeva et al, 2013; Tveit et al, 2013; Moore et al, 2015; Ivanova et al, 2016). Although several peat-inhabiting planctomycetes have been obtained in pure cultures (Dedysh and Kulichevskaya, 2013), we know very little about their potential functions in the environment.…”

High Diversity of Planctomycetes in Soils of Two Lichen-Dominated Sub-Arctic Ecosystems of Northwestern Siberia

“…Sphagnum -dominated boreal wetlands represent one of the most extensive terrestrial low-temperature environments where members of the Planctomycetes are especially widespread and abundant (Dedysh et al, 2006; Kulichevskaya et al, 2006; Bragina et al, 2012, 2015; Ivanova and Dedysh, 2012; Serkebaeva et al, 2013; Moore et al, 2015; Ivanova et al, 2016). The predominant planctomycete populations in northern wetlands are represented by members of the phylogenetic group defined by the genera Isosphaera and Singulisphaera (Ivanova and Dedysh, 2012; Serkebaeva et al, 2013; Moore et al, 2015).…”