Genomics and metatranscriptomics of biogeochemical cycling and degradation of lignin-derived aromatic compounds in thermal swamp sediment

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.

Microbial Roles in Dissolved Organic Matter Transformation in Full-Scale Wastewater Treatment Processes Revealed by Reactomics and Comparative Genomics

“…DOM transformation by microbes mainly initiates from liable fractions’ (e.g., aliphatic compounds) degradation by extracellular enzymes (e.g., amylase) that display a broad substrate specificity. , Microbes consume liable fractions to produce recalcitrant (e.g., lignin-like) substances that have decreased molecular weight and unsaturation and increased aromaticity . Consequently, chitinase, esterase, laccases, peroxidases, glyoxal oxidase, and phenolic acid decarboxylase catalyze ring cleavage, oxidation, and decarboxylation for recalcitrant DOM degradation. In complex ecosystems, microbes often occupy different niches and show taxon-specific metabolic affinities with different DOM fractions. − Gamma- and Delta-proteobacteria clades harbor well-known taxa (e.g., Geobacter and Psychromonas ) that prefer simple DOM compounds. , In contrast, microbes from Chloroflexi and Crenarchaeota are observed to degrade more recalcitrant and aromatic compounds .…”

Distribution Characteristics of C–N–S Microorganism Genes in Different Hydraulic Zones of High-Rank Coal Reservoirs in Southern Qinshui Basin

“…In this case, the high-rank coal in the study area was difficult to degrade, the degradation of recalcitrant C from the surface would be an important substrate for microorganisms, and the monosaccharide produced could have further provided substrates for carbohydrate metabolism. 10 , 26 , 27 The genes associated with mannose metabolism, carbohydrate hydrolases, lactose and galactose uptake and utilization, l -fructose utilization, xylose utilization, and chitin utilization, were all higher in the stagnant area ( Figure S1 ). Overall, as these functional genes directly participate in C degradation, their higher abundance could enhance C decomposition and enhance methanogenesis and other anaerobic heterotrophic microorganisms, such as nitrate-reducing bacteria and sulfate-reducing bacteria.…”

“…Breakdown of polysaccharides into simple sugars is the primary source of energy and carbon for the microbial community. 10,26,27 Degradation pathways for monosaccharides, glucose, galactose, and xylose were also prevalent in the Picrust2 data, including the genes associated with mannose metabolism, carbohydrate hydrolases, lactose and galactose uptake and utilization, L-fructose utilization, and xylose utilization. 56 In anaerobic coal reservoirs, especially in stagnant areas, inorganic terminal electron acceptors (nitrate and sulfate) are rare, and fermentation and acetogenesis are essential pathways for the further degradation of monosaccharides and to supply substrates for methanogenesis.…”

Microbial community and performance of a partial nitritation/anammox sequencing batch reactor treating textile wastewater

“…NGS analysis further confirmed that the granules community was dominated by heterotrophic, nitrifying and denitrifying genera suggesting that shortcut nitrification-denitrification instead of PN/A process was established since the first weeks of operation. Chryseobacterium (genera containing species both capable of heterotrophic nitrification and aerobic denitrification [ 54 , 55 ]) was the most common genera (7.7–27.2%), while other dominant genera were Hylemonella (7.3–13.9%, denitrifiers [ 56 ]), followed by Nitrosomonas (9.9–14.0%, mainly nitrifiers [ 57 ]), Parvibaculum (7.0–11.7%, aerobic hydrocarbon-degrading bacteria and denitrifiers [ 58 , 59 ]), Rubrivivax (3.3–15.7%, involved in multiple biogeochemical and aromatic transformations, also denitrification, due to a wide metabolic capacity [ 58 , 60 ]) and other Comamonadaceae (4.3–8.9%, aromatic degraders and denitrifiers [ 61 ]), Chitinophagaceae (3.6–10.9%), other Saphrospirales (0.1–9.4%), Sphingopyxis (2.2–4.7%), other Burkholderiales (2.1–4.3%), Bdellovibrio (0.7–2.9%), Diaphorobacter (1.2–2.2%, both heterotrophic nitrifiers and denitrifiers [ 62 ]), Rhodanobacter (1.0–1.6%), the families of Alcaliganaceae (0.7–1.7%) and Xanthomonadaceae (0.8–1.1%), Clostridium (0.3–1.3%, biopolymers degraders able of N fixation [ 63 , 64 ]), Thermomonas (0.6–1.0%, denitrifiers [ 65 , 66 ]), Pseudomonas (0.0–1.4%, capable of both heterotrophic nitrification and/or aerobic denitrification [ 67 ]), and the family of Bradyrhizobiaceae (0.2–1.0%, N fixation [ 68 ]), other bacteria that singularly accounted for less than 1% of the total abundance were 7.6–14.3%.…”