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Evolution and Classification of GH101 Family Glycoside Hydrolases: Four Years Later Daniil G. Naumoff
S. N. Winogradsky Institute of Microbiology, Russian Academy of Sciences, Prospekt 60-letiya Oktyabrya 7/2, Moscow 117312, Russia; daniil_naumoff@yahoo.com

Recent progress in geno me sequencing resulted in a rapid growth of the sequence databases. The number of known representatives of all protein families has increased dramat ically. It naturally raises a quest ion if the exist ing protein classificat ions are still stable or appearance of «the intermediate forms» washed out the clear borders between protein families or subfamilies. As a case study, we choose family GH101 of glycoside hydrolases. On the basis of sequence similarit y of the catalyt ic domains all glycoside hydro lases have been grouped into more than 100 families (GH1-GH131). Family GH101 includes retaining endo--N-acetylgalactosaminidases (EC 3.2.1.97) and their uncharacterized ho mologues (totally 100 proteins) [1]. This family was described in 2005 [2]. Four years ago we revealed 95 non-ident ical protein sequences o f GH101 domains from GenPept database using the blast algorithm [3]. These sequences represented 18 genera of bacteria fro m Actinobacteria, Bacteroidetes, Firmicutes, and Verrucomicrobia. Pairwise sequence alignment and phylogenet ic analysis allowed us to distinguish six subfamilies (101a-101f) in the GH101 family. Iterative screening of the protein database by PSI-BLAST revealed the closest relat ionship of GH101 domains wit h GH129 (or GHL1) domains. More distant similarit y was found with so me proteins from GH13, GH20, GH27, GH29, GH31, GH36, GH66, GH70, GH97, COG1306, and COG1649 families [3-5]. Recent ly we did another analysis o f the GenPept database. Iterative screening of the database allowed us to reveal more than 15,000 proteins homo logous to GH101 domains. They represent several families of glycoside hydrolases having the TIM-barrel type catalyt ic domains. Particularly we found 345 proteins containing the GH101 domain. This family is still quite dist inct and its closest neighbor is GH129 family o f -N-acet ylgalactosaminidases


(EC 3.2.1.49). In order to additionally increase the number of proteins for phylogenet ic analys is we also used 17 GH101-containing proteins found in the Integrated Microbial Geno mes database [6]. All obtained proteins belo ng to the same four bacterial phyla as four years ago with clear do mination of representatives fro m Actinobacteria and Firmicutes. We found no GH101-containing proteins fro m Proteobacteria despite the fact that almost a half of all bacterial geno me projects corresponds to this phylum [7]. According to the phylogenet ic analysis, the subfamily structure retains stable: almost all proteins can be easily classified in six subfamilies described by us four years ago [3]. All subfamilies compose stable clusters on the tree. In contrast to many other glycoside hydro lase families, the role o f lateral gene transfers and gene duplications was minor during the evo lut ion of genes encoding GH101-containing proteins.

1. The Carbohydrate-Act ive Enzymes Database [http://www.cazy.org/]. 2. K. Fujita et al. (2005) Identificat ion and mo lecular cloning of a novel glycoside hydro lase family o f core 1 type O-glycan-specific endo--N-acetylgalactosaminidase from Bifidobacterium longum, J. Biol. Chem., 280:37415­37422. 3. D.G. Naumo ff (2009) Sequence analysis o f endo--N-acetylgalactosaminidases and their ho mo logues, Proceedings of the International Moscow Conference on Computational Molecular Biology (MCCMB'09), July 20-23, 2009, Moscow, Russia, P.251­252 [http://mccmb.belozersky.msu.ru/2009/MCCMB09_Proceedings.pdf]. 4. D.G. Naumo ff (2009) Sequence analysis o f endo--N-acetylgalactosaminidases, Glycoconjugate J., 26:847. 5. D.G. Naumo ff (2010) GH101 family o f glycoside hydrolases: Subfamily structure and evo lut ionary connect ions with other families, J. Bioinform. Comput. Biol., 8:437­451. 6. The Integrated Microbial Geno mes [https://img.jgi.doe.gov/]. 7. The Genomes On-Line Database [http://www.geno mesonline.org/].