Abstract
Lignin is a recalcitrant macromolecule formed by three alcohols (monolignols) predominantly connected by β-aryl ether linkages and is one of the most abundant organic macromolecules in the biosphere. However, the role played by environmental bacteria in lignin degradation is still not entirely understood. In this study, we identified an environmental Klebsiella strain isolated from sediment collected from an altitudinal region in a unique Brazilian biome called Caatinga. This organism can also grow in the presence of kraft lignin as a sole source of carbon and aromatic compounds. We performed whole-genome sequencing and conducted an extensive genome-based metabolic reconstruction to reveal the potential mechanisms used by the bacterium Klebsiella variicola P1CD1 for lignin utilization as a carbon source. We identified 262 genes associated with lignin-modifying enzymes (LMEs) and lignin-degrading auxiliary enzymes (LDAs) required for lignin and aromatic compound degradation. The presence of one DyP (Dye-decolorizing Peroxidase) gene suggests the ability of P1CD1 strain to access phenolic and nonphenolic structures of lignin molecules, resulting in the production of catechol and protocatechuate (via vanillin or syringate) along the peripheral pathways of lignin degradation. K. variicola P1CD1 uses aldehyde-alcohol dehydrogenase to perform direct conversion of vanillin to protocatechol. The upper funneling pathways are linked to the central pathways of the protocatechuate/catechol catabolic branches via β-ketoadipate pathways, connecting the more abundant catabolized aromatic compounds with essential cellular functions, such as energy cellular and biomass production (i.e., via acetyl-CoA formation). The combination of phenotypic and genomic approaches revealed the potential dissimilatory and assimilatory ability of K. variicola P1CD1 to perform base-catalyzed lignin degradation, acting on high- and low-molecular-weight lignin fragments. These findings will be relevant for developing metabolic models to predict the ligninolytic mechanism used by environmental bacteria and shedding light on the flux of carbon in the soil.
Highlights
Microorganisms are essential in the cycling of a wide range of molecules in the environment, playing critical roles in biogeochemical cycles, and are essential in promoting the balance of life
K. variicola P1CD1 was isolated in the presence of alkali lignin as the sole carbon source and in the presence of kraft lignin in solid and liquid media
A semi-quantitative approach was used to detect the conversion of kraft lignin in microbial biomas. we weighed the residual lignin in the absence and presence of the K. variicola P1CD1 strain after 96 hours of growth
Summary
Microorganisms are essential in the cycling of a wide range of molecules in the environment, playing critical roles in biogeochemical cycles, and are essential in promoting the balance of life. Among the main activities are those associated with environmental organic carbon cycling. Lignocellulosic biomass represents the most abundant organic compound of vegetal origin on the planet. The degradation of lignocellulosic biomass in the environment represents one of the main routes of cycling organic carbon in terrestrial ecosystems. The possible arrangements among these units generate a diversity of polymeric structures and vary according to different plant species, resulting in distinct stiffness levels in the plant structure [2]. This diverse and complex panel of molecular arrangements results in structures resistant to various microbial enzymes, causing their environmental recalcitrance. The lignin degradation process requires a system of enzymes specialized in the attack of specific chemical groups that perform polymer deconstruction in a concerted and ordered way to result in mineralization of the molecule
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