Abstract
Thermal swamps are unique ecosystems where geothermally warmed waters mix with decomposing woody biomass, hosting novel biogeochemical-cycling and lignin-degrading microbial consortia. Assembly of shotgun metagenome libraries resolved 351 distinct genomes from hot-spring (30–45 °C) and mesophilic (17 °C) sediments. Annotation of 39 refined draft genomes revealed metabolism consistent with oligotrophy, including pathways for degradation of aromatic compounds, such as syringate, vanillate, p-hydroxybenzoate, and phenol. Thermotolerant Burkholderiales, including Rubrivivax ssp., were implicated in diverse biogeochemical and aromatic transformations, highlighting their broad metabolic capacity. Lignin catabolism was further investigated using metatranscriptomics of sediment incubated with milled or Kraft lignin at 45 °C. Aromatic compounds were depleted from lignin-amended sediment over 148 h. The metatranscriptomic data revealed upregulation of des/lig genes predicted to specify the catabolism of syringate, vanillate, and phenolic oligomers in the sphingomonads Altererythrobacter ssp. and Novosphingobium ssp., as well as in the Burkholderiales genus, Rubrivivax. This study demonstrates how temperature structures biogeochemical cycling populations in a unique ecosystem, and combines community-level metagenomics with targeted metatranscriptomics to identify pathways with potential for bio-refinement of lignin-derived aromatic compounds. In addition, the diverse aromatic catabolic pathways of Altererythrobacter ssp. may serve as a source of thermotolerant enzymes for lignin valorization.
Highlights
Few geothermally influenced wetlands exist on Earth— geothermal hot springs that feed marshlands can be found in Yellowstone National Park (USA) [1,2,3], Great Rift Valley (Kenya), Iceland, and New Zealand [4]—fewer still are forested
Thermotolerant Alphaproteobacteria and Gammaproteobacteria from a geothermal environment expressed aromatic degradation pathways for lignin-derived monoaromatic compounds and aromatic oligomers in incubation with lignin. This finding is highly relevant to understanding the ecology of carbon cycling in geothermal environments, and has substantial biotechnology implications
The syringate meta-cleavage pathway was primary expressed on eucalyptus kraft lignin (EKL), which contained about three times higher concentration of dimethoxylated S-lignin-derived substrates than Glignin monomers
Summary
Few geothermally influenced wetlands exist on Earth— geothermal hot springs that feed marshlands can be found in Yellowstone National Park (USA) [1,2,3], Great Rift Valley (Kenya), Iceland, and New Zealand [4]—fewer still are forested. Canada feature geothermally warmed springs (30–55 °C) with organic sediments and biomats that receive inputs from the surrounding mixed-forest vegetation. Based on these characteristics, we hypothesized that this environment harbors thermotolerant microbiota capable of degrading lignin-derived aromatic compounds. Due to the convergent organization of bacterial catabolic pathways, they are well suited to the biocatalytic conversion of these biomass-derived aromatics to fuels and chemicals [16,17,18]. Genomic reconstruction revealed diverse chemoautotrophic metabolism in the thermal microbiome but only partially elucidated aromatic pathways for lignin-derived compounds, while metatranscriptomics and analytical chromatography provided evidence for thermotolerant catabolism of aromatic compounds. This study characterized transcriptomes from oligotrophic sphingomonads associated with degradation of S- and G-lignin at elevated temperature
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