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Peroxidase Evolution in White-Rot Fungi Follows Wood Lignin Evolution in Plants

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Peroxidase Evolution in White-Rot Fungi Follows Wood Lignin Evolution in Plants Peroxidase evolution in white-rot fungi follows wood lignin evolution in plants Iván Ayuso-Fernándeza, Jorge Rencoretb, Ana Gutiérrezb, Francisco Javier Ruiz-Dueñasa, and Angel T. Martíneza,1 aCentro de Investigaciones Biológicas, Consejo Superior de Investigaciones Científicas, E-28040 Madrid, Spain; and bInstituto de Recursos Naturales y Agrobiología de Sevilla, Consejo Superior de Investigaciones Científicas E-41012 Seville, Spain Edited by David M. Hillis, The University of Texas at Austin, Austin, TX, and approved July 25, 2019 (received for review March 23, 2019) A comparison of sequenced Agaricomycotina genomes suggests peroxidases and analyzed their evolution in Polyporales using that efficient degradation of wood lignin was associated with the high– and low–redox potential simple model substrates (11). appearance of secreted peroxidases with a solvent-exposed cata- These studies suggest that the most ancestral ligninolytic en- lytic tryptophan. This hypothesis is experimentally demonstrated zymes acted on phenolic lignin and later shaped their oxidation here by resurrecting ancestral fungal peroxidases, after sequence sites several times to become first VPs and later LiPs, the most reconstruction from genomes of extant white-rot Polyporales, and efficient lignin-degrading enzymes, as a convergent trait in fungal evaluating their oxidative attack on the lignin polymer by state-of- evolution (12). Also, ligninolytic peroxidases progressively in- the-art analytical techniques. Rapid stopped-flow estimation of the transient-state constants for the 2 successive one-electron transfers creased the redox potential of their reactive species (13). Finally, their stability at acidic pH, where lignin decay takes place in from lignin to the peroxide-activated enzyme (k2app and k3app) showed a progressive increase during peroxidase evolution (up to nature, increased, and their catalytic tryptophan environment 50-fold higher values for the rate-limiting k3app). The above agreed became more negative to stabilize lignin cation radicals (11, 12). with 2-dimensional NMR analyses during steady-state treatments of Recent phylogenomic studies on over 1,000 Agaricomycetes hardwood lignin, showing that its degradation (estimated from the suggest that during evolution wood-rotting fungi became host normalized aromatic signals of lignin units compared with a control) specific depending on whether they were brown-rot fungi, often and syringyl-to-guaiacyl ratio increased with the enzyme evolution- acting on conifers, or white-rot fungi, specializing on angiosperms EVOLUTION ary distance from the first peroxidase ancestor. More interestingly, (14). The evolution of host specialization is notably interesting the stopped-flow estimations of electron transfer rates also showed since conifer lignin basically consists of guaiacyl (G) units, while how the most recent peroxidase ancestors that already incorporated angiosperms introduce also syringyl (S) units, with minor amounts the exposed tryptophan into their molecular structure (as well as the of p-hydroxyphenyl (H) units in both lignins, as illustrated in Fig. 1 extant lignin peroxidase) were comparatively more efficient at oxi- (see SI Appendix,TableS1, for a comprehensive review of lignin dizing hardwood (angiosperm) lignin, while the most ancestral “tryptophanless” enzymes were more efficient at abstracting elec- composition). As shown in Fig. 1, S-type units were also incor- trons from softwood (conifer) lignin. A time calibration of the ances- porated by some nonconifer gymnosperms and a few ferns and try of Polyporales peroxidases localized the appearance of the first lycophytes as an example of convergent evolution discussed below. peroxidase with a solvent-exposed catalytic tryptophan to 194 ± 70 Lignin in conifers did not show detectable changes during evolu- Mya, coincident with the diversification of angiosperm plants char- tion (15). Then, the general inclusion of S units in angiosperms acterized by the appearance of dimethoxylated syringyl lignin units. Significance fungal evolution | lignin evolution | ancestral peroxidases | stopped-flow spectrophotometry | NMR spectroscopy We analyze the evolution of ligninolytic peroxidases from wood-rotting fungi using conifer and angiosperm lignin as ignin is an aromatic polymer formed by dehydrogenative representatives of 2 steps of lignin evolution. By enzyme res- Lcoupling of p-hydroxycinnamyl alcohols and other phenols (1) urrection, we show that during fungal evolution, these en- that confers resistance and other properties to vascular plants. zymes improved their activity and switched their degradative Due to lignin recalcitrance, its degradation is essential for carbon preferences with the rise of a surface tryptophan conferring on recycling in nature and often represents a limiting step for a them the ability to oxidize nonphenolic lignin. We calibrated biobased economy (2). The biological degradation of lignin is the peroxidase phylogeny and determined that this residue described as an enzymatic combustion (3) typically made by appeared coincident with angiosperm diversification, charac- Polyporales and other white-rot Agaricomycetes. It involves the terized by the synthesis of a more complex and less phenolic so-called manganese peroxidases (MnPs), versatile peroxidases lignin due to the general incorporation of a new unit in its (VPs), and lignin peroxidases (LiPs) together with auxiliary en- structure. This way, we show that fungal evolution followed zymes (4). MnPs oxidize the often minor phenolic moiety of that of lignin synthesis, pointing to a coevolution between + lignin via Mn3 chelates or directly at the heme cofactor (5). In fungal saprotrophs and their plant hosts. contrast, LiPs attack nonphenolic lignin directly using a solvent- exposed catalytic tryptophan forming a reactive radical, as shown Author contributions: F.J.R.-D. and A.T.M. designed research; I.A.-F. and J.R. performed research; A.G. contributed new reagents/analytic tools; I.A.-F., F.J.R.-D., and A.T.M. ana- using model compounds (6). Finally, VPs combine the structural lyzed data; I.A.-F. performed bioinformatic analysis; and I.A.-F., F.J.R.-D., and A.T.M. wrote and catalytic properties of MnPs and LiPs (7), including the the paper. surface tryptophan, whose role in direct oxidation of lignin was The authors declare no conflict of interest. recently demonstrated (8). This article is a PNAS Direct Submission. Fungal degradation of lignin via white rot arose around the This open access article is distributed under Creative Commons Attribution-NonCommercial- Carboniferous period, associated with the production of the first NoDerivatives License 4.0 (CC BY-NC-ND). ligninolytic peroxidases (9) and, along with geochemical factors, 1To whom correspondence may be addressed. Email: [email protected]. may have contributed to the decline of carbon sequestration This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. (coal formation) toward the end of the Permo-Carboniferous 1073/pnas.1905040116/-/DCSupplemental. period (10). Recent works have resurrected ancestral ligninolytic www.pnas.org/cgi/doi/10.1073/pnas.1905040116 PNAS Latest Articles | 1of6 A B C D water solubility, a requisite for the above stopped-flow analyses. H H H H These preparations originate from sulfite pulping of wood, a S S S G process based on lignin sulfonation (19). While solubilizing lig- G G G nin, sulfonation scarcely affects peroxidase reactivity (18). Here we investigate how ancestral peroxidases modify lignin through their evolution and estimate the electron transfer rates from Fig. 1. Average lignin composition (H, G, and S molar content) in angio- sperms (A), conifers (B), other gymnosperms (C), and ferns and lycophytes softwood and hardwood lignosulfonates. With this purpose, we (D) from a total of 144 species (see SI Appendix, Table S1, for the complete use stopped-flow rapid spectrophotometry to calculate transient- inventory). state kinetic parameters and 2-dimensional (2D) NMR spec- troscopy to evaluate the polymer modification in extended steady-state treatments. resulted in a more complex lignin providing mechanical and physiological advantages to plants (16, 17). Results So far, the evolution of ancestral peroxidase has not been Evolution of Polyporales Lignin-Degrading Peroxidases. To investi- analyzed using the lignin polymer as a substrate since initial rates gate how the ability to oxidize the lignin polymer evolved in the of lignin oxidation cannot be obtained under steady-state con- ancestry of Polyporales peroxidases (20), we reconstructed with ditions. However, the electron transfer rates can be accurately PAML the lineage leading to the well-known isoenzyme H8 of estimated from the reduction of peroxide-activated enzymes by Phanerochaete chrysosporium LiP, corresponding to gene A in the lignin under stopped-flow conditions (8, 18). Among available sequenced genome (PC-LiPA) (21). Then, we resurrected by lignin preparations, lignosulfonates are unique because of their Escherichia coli expression (11) the main nodes in the evolutionary BJEAD-LiP (12) ALiP PC-LiPA PHACH-LiP (10) PHLBR-LiP (5) AVPd TRAVE-LiP (10) Clade D TRAVE-43289-VP GANSP-116056-VP TRAVE-MnPshort (7) DICSQ-MnPshort (2) GANSP-142454-MnPshort TRAVE-112835-MnPshort BJEAD-MnPshort (2) PHLBR-MnPshort (2) BJEAD-43095-VP BJEAD-306404-MnPshort GANSP-176788-MnPshort TRAVE-43477-MnPshort CERSU-124076-MnPshort CERSU-118677-LiP CaD CERSU-99382-VP BJEAD-173495-GP BJEAD-43329-MnPshort
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