Evolutionary convergence in lignin-degrading enzymes

Abstract

SignificanceWe analyze the molecular mechanisms that led to the rise of a powerful strategy for lignin degradation (i.e., the formation of a solvent-exposed tryptophanyl radical capable of oxidizing the bulky lignin polymer) as a convergent trait in different species of fungi (order Polyporales). We use ancestral sequence reconstruction and enzyme resurrection to obtain the ancestors of the two extant types of ligninolytic peroxidases—lignin peroxidase (LiP) and versatile peroxidase (VP)—and compare their predicted molecular structures and catalytic properties after resurrection. The results presented demonstrate convergent evolution in distant LiP and VP lineages with the exposed tryptophan residue appearing twice, as two independent events, following different molecular changes.

Increase of Redox Potential during the Evolution of Enzymes Degrading Recalcitrant Lignin

“…The evolutionary changes in ligninolytic peroxidases have been recently investigated by resurrection of ancestral enzymes from sequenced genomes of Polyporales, in which most lignin‐degrading fungi are included. In this way, the transition from an ancestor that oxidized lignin poorly using diffusible Mn 3+ chelates, around 400 million years ago, into more efficient enzymes that oxidized lignin directly was demonstrated .…”

“… Representation of the evolutionary distance of the ancestral and extant enzymes (Ref. ) using the chemical shift ( δ H ) of signal Z in the 1 H NMR spectra of their CN adducts, which is shown in Figure .…”

“…[5] Lignin biodegradation, which was defined as an enzymatic combustion, [6] is ak ey step for carbon recycling in land ecosystemsa nd ap rocesso fb iotechnological interestf or the use of plant biomass in ab io-based economy. [7,8] The evolutionary changes in ligninolytic peroxidases have been recently investigated [9,10] by resurrection of ancestral enzymesf rom sequenced genomes of Polyporales, [11] in which most lignin-degrading fungi are included. In this way,t he transition from an ancestor that oxidized lignin poorly using diffusible Mn 3 + chelates, around4 00 millionyears ago, [12] into more efficient enzymes that oxidized lignin directly was demonstrated.…”

“…In particular,t he more than five-fold higher efficiency of PC-LiPAo xidizingt he simple lignin model compound veratryl alcoholc an be connected with the above environment, which is more negative than in its ancestors. [10] Therefore, it seemst hat, once ah igh enoughr eduction potential had been attained( in ALiP), the peroxidase final evolutionary step focused on increasing the acidic stabilitya nd selecting a more acidic tryptophanyl radical environment in extantL iP.A s aw hole, ancestral enzymer esurrection illustrates how LiPs becamethe most efficient enzymes degrading lignin.…”

“…E8' values for the three redox couples in the catalytic cycle (Figure2)v ersus evolutionary distance (seeRef [10]…”