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

Abstract

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 × 10 15 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 th...

Biochemical Investigations of Five Recombinantly Expressed Tyrosinases Reveal Two Novel Mechanisms Impacting Carbon Storage in Wetland Ecosystems

“…In terms of activity (k cat values), diphenols are preferred over monophenols, which is in accordance with previous reports. 4,29 When comparing the k cat values of corresponding mono-and diphenols (tyramine− dopamine, L-tyrosine−L-DOPA, p-coumaric acid−caffeic acid, p-hydroxybenzoic acid−protocatechuic acid; Figure S1), all investigated enzymes showed higher activity levels toward the diphenolic substrate, compared to the corresponding monophenolic substrate (Table 2). This trend is in accordance with literature-reported kinetic investigations of bacterial TYRs.…”

“…Enzymes capable of oxidatively removing phenolic compounds in the presence of molecular oxygen (or H 2 O 2 for peroxidases) are often grouped under the umbrella term "phenol oxidases", and include, among others, tyrosinases, laccases, and peroxidases. 4 In wetlands, the activity of phenol oxidases (and thus the removal of phenolic compounds) is restricted by oxygen scarcity, resulting from water-logging. 13 Climate change, which will lead to increased temperatures and reduced rainfall, threatens water tables in wetlands and will, therefore, promote the aeration of previously anoxic wetland soils.…”

“…A recent review showed that a variety of bacteria (including Acidobacteria, Actinobacteria, Bacteroidetes, Firmicutes, Nitrospirae, Planctomycetes, and Proteobacteria) capable of producing tyrosinase enzymes (TYRs) are present in globally distributed wetland ecosystems (including peatlands, marshes, mangrove forests, bogs, and alkaline soda lakes). 4 Thus, it has been concluded that TYRs are among the key enzymes controlling carbon cycling within wetland ecosystems (besides laccases, peroxidases, and enzymes involved in anoxic phenol metabolism). 4 The relative impacts of TYRs, laccases, peroxidases, and enzymes involved in anoxic phenol metabolism on carbon cycling in wetland ecosystems require further investigation.…”

“…, β-glucosidases, peroxidases, xylosidases, and chitinases) − by phenolic compounds. Phenolic compounds act as unspecific enzyme inhibitors and are naturally abundant within wetland ecosystems , due to plant secondary metabolism. Enzymes capable of oxidatively removing phenolic compounds in the presence of molecular oxygen (or H 2 O 2 for peroxidases) are often grouped under the umbrella term “phenol oxidases”, and include, among others, tyrosinases, laccases, and peroxidases .…”

“…Wetlands are ecosystems characterized by permanently or seasonally water-logged soils in combination with plant growth. , For most types of wetlands (peatlands, mangrove forests, bogs, and marshes), high levels of phenolic compounds have been reported. , Wetlands represent unbalanced ecosystems in which the rate of carbon sequestration from the atmosphere ( via the Calvin cycle of plant photosynthesis) exceeds the rate of carbon release, predominantly as CO 2 and CH 4 . , Thus, they have accumulated vast amounts of carbon over the last millennia. While wetlands cover only 5–8% of the terrestrial land surface, they are estimated to store 20–30% (500–550 × 10 15 g) of the global soil carbon pool, which is equivalent to 66–72% of the entire atmospheric carbon pool of 760 × 10 15 g. ,− Within recent years, the so-called “latch mechanism” has been established to explain how wetlands act as long-term carbon sinks (Figure A).…”