The Novel Role of Tyrosinase Enzymes in the Storage of Globally Significant Amounts of Carbon in Wetland Ecosystems

Over the last millennia, wetlands have been sequestering carbon from the atmosphere via photosynthesis at a higher rate than releasing it and, therefore, have globally accumulated 550 x 1015 g of carbon, which is equivalent to 73% of the atmospheric carbon pool. The accumulation of organic carbon in wetlands is effectuated by phenolic compounds, which suppress the degradation of soil organic matter by inhibiting the activity of organic-matter-degrading enzymes. The enzymatic removal of phenolic compounds by bacterial tyrosinases has historically been blocked by anoxic conditions in wetland soils, resulting from waterlogging. Bacterial tyrosinases are a subgroup of oxidoreductases that oxidatively remove phenolic compounds, coupled to the reduction of molecular oxygen to water. The biochemical properties of bacterial tyrosinases have been investigated thoroughly in vitro within recent decades, while investigations focused on carbon fluxes in wetlands on a macroscopic level have remained a thriving yet separated research area so far. In the wake of climate change, however, anoxic conditions in wetland soils are threatened by reduced rainfall and prolonged summer drought. This potentially allows tyrosinase enzymes to reduce the concentration of phenolic compounds, which in turn will increase the release of stored carbon back into the atmosphere. To offer compelling evidence for the novel concept that bacterial tyrosinases are among the key enzymes influencing carbon cycling in wetland ecosystems first, bacterial organisms indigenous to wetland ecosystems that harbor a TYR gene within their respective genome (tyr(+)) have been identified, which revealed a phylogenetically diverse community of tyr(+ )bacteria indigenous to wetlands based on genomic sequencing data. Bacterial TYR host organisms covering seven phyla (Acidobacteria, Actinobacteria, Bacteroidetes, Firmicutes, Nitrospirae, Planctomycetes, and Proteobacteria) have been identified within various wetland ecosystems (peatlands, marshes, mangrove forests, bogs, and alkaline soda lakes) which cover a climatic continuum ranging from high arctic to tropic ecosystems. Second, it is demonstrated that (in vitro) bacterial TYR activity is commonly observed at pH values characteristic for wetland ecosystems (ranging from pH 3.5 in peatlands and freshwater swamps to pH 9.0 in soda lakes and freshwater marshes) and toward phenolic compounds naturally present within wetland environments (p-coumaric acid, gallic acid, protocatechuic acid, p-hydroxybenzoic acid, caffeic acid, catechin, and epicatechin). Third, analyzing the available data confirmed that bacterial host organisms tend to exhibit in vitro growth optima at pH values similar to their respective wetland habitats. Based on these findings, it is concluded that, following increased aeration of previously anoxic wetland soils due to climate change, TYRs are among the enzymes capable of reducing the concentration of phenolic compounds present within wetland ecosystems, which will potentially destabilize vast amounts of carbon stored in these ecosystems. Finally, promising approaches to mitigate the detrimental effects of increased TYR activity in wetland ecosystems and the requirement of future investigations of the abundance and activity of TYRs in an environmental setting are presented.

Automated summary

Wetlands have accumulated a significant amount of carbon over the past millennia, with phenolic compounds playing a key role in inhibiting soil organic matter degradation. Climate change threatens to alter anoxic conditions in wetland soils, potentially impacting the release of stored carbon back into the atmosphere.