Chapter 2 Molecular Phylogeny of Heme Peroxidases

All currently available gene sequences of heme peroxidases can be phylogenetically divided in two superfamilies and three families. In this chapter, the phylogenetics and genomic distribution of each group are presented. Within the peroxidase–cyclooxygenase superfamily, the main evolutionary direction developed peroxidatic heme proteins involved in the innate immune defense system and in biosynthesis of (iodinated) hormones. The peroxidase–catalase superfamily is widely spread mainly among bacteria, fungi, and plants, and particularly in Class I led to the evolution of bifunctional catalase–peroxidases. Its numerous fungal representatives of Class II are involved in carbon recycling via lignin degradation, whereas Class III secretory peroxidases from algae and plants are included in various forms of secondary metabolism. The family of di-heme peroxidases are predominantly bacteria-inducible enzymes; however, a few corresponding genes were also detected in archaeal genomes. Four subfamilies of dyp-type peroxidases capable of degradation of various xenobiotics are abundant mainly among bacteria E. Torres and M. Ayala (eds.), Biocatalysis Based on Heme Peroxidases, DOI 10.1007/978-3-642-12627-7_2, # Springer-Verlag Berlin Heidelberg 2010 7 and fungi. Heme-haloperoxidase genes are widely spread among sac and club fungi, but corresponding genes were recently found also among oomycetes. All described families herein represent heme peroxidases of broad diversity in structure and function. Our accumulating knowledge about the evolution of various enzymatic functions and physiological roles can be exploited in future directed evolution approaches for engineering peroxidase genes de novo for various demands. 2.1 Systematic Classification of Peroxidases It is already well established that peroxidases are ubiquitous and abundant enzymes in all forms of life. Even in strictly anaerobic bacteria [1, 2], hydroperoxidases play an essential function mainly in signaling and maintaining oxygen tolerance. Primordial blue-green algae (i.e., cyanobacterial predecessors) that appeared about 3.2 billion years ago must have been among the first organisms that elaborated mechanisms for the detoxification of partially reduced, reactive oxygen species as a consequence of their oxygen-evolving photosystem [3]. A significant increase in the level of atmospheric oxygen at the beginning of Proterozoic (i.e., between 2.45 and 2.32 billion years ago) [4] necessarily led to further sophisticated evolution of both prokaryotic and eukaryotic antioxidative stress responses, with peroxidases and catalases being among the most prominent enzymatic factors [5]. The genome sequencing projects of last two decades have shed light on the presence of numerous gene orthologs and paralog variants of heme peroxidase gene families in almost all known genomes. The full-length coding sequences (both DNA and amino acids) are the base for any comprehensive higher-level phylogenetic reconstruction, and with increasing number and reliability of sequence data, our evolutionary views are improving. We have attempted to collect all available peroxidase sequences in the PeroxiBase [6] http://peroxidase.isb-sib.ch. Out of 6,861 known peroxidase sequences collected in PeroxiBase (January 2010), more than 73% of them code for heme-containing peroxidases. In the majority of cases, heme b is the prosthetic group, and its evolutionary highly conserved amino acid surroundings influences its reactivity. All currently known heme-containing peroxidases can be divided in two main superfamilies and three families. Contrary to some recently published opinions [7], the in-depth phylogenetic analysis clearly reveals that almost all of these heme peroxidase coding genes have very ancient prokaryotic origins probably dating back to the rise of atmospheric oxygen. All (super)families described below represent their own peculiar mode of evolution in maintaining and regulating the heme reactivity. The classical division into plant and animal heme peroxidases nowadays appears to be obsolescent and not appropriate. There are numerous examples of interkingdom distribution for members of most herein described gene families. It is therefore more suitable to name the appropriate groupings according to peculiar reaction specificity in each observed (super)family. As a special case of hydroperoxidases, heme-containing catalases represent a very abundant gene family [8, 9], but they will not be analyzed in this contribution as they dominantly exhibit catalatic 8 M. Zámocký and C. Obinger