Comparative genomics of carbohydrates utilization in bacteria of the family Sphaerochaetaceae: evolutionary origin of the genes encoding galacturonidase and unsaturated rhamnogalacturonyl hydrolase

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Abstract

A comparative analysis of carbohydrate degradation proteins encoded in currently available genomic sequences of bacteria of the family Sphaerochaetaceae, namely Sphaerochaeta associata GLS2T, S. globosa BuddyT, S. pleomorpha GrapesT, S. halotolerans 4-11T, S. halotolerans 585, Sphaerochaeta sp. S2, Sphaerochaeta sp. PS and Parasphaerochaeta coccoides SPN1T was carried out. The genomes of Sphaerochaeta spp. encode a medium-sized and diverse set of proteins potentially involved in the degradation of different classes of carbohydrates, mainly oligosaccharides. All studied genomes encode glycoside hydrolases of the GH1, GH2, GH3, GH4, GH13, GH20, GH28, GH36, GH43, GH57, GH63, GH77 and GH105 families, as well as carbohydrate esterases of the CE8 and CE9 families. All studied bacteria, with the exception of P. coccoides SPN1T, have many proteins of the GH31 family encoded in their genomes. The studied representatives of Sphaerochaetaceae do not have genes coding for endo-β-acetylmuramidase (lysozyme) of the GH23 family involved in the process of peptidoglycan turnover. However, the genomes of S. associata, S. globosa, Sphaerochaeta sp. PS and S. pleomorpha contain the exo-β-acetylmuramidase gene (GH171 family). A significant part of the genes encoding carbohydrate degradation enzymes have the closest homologues among representatives of the phyla Bacillota, Bacteroidota, and Pseudomonadota. The genomes of the studied bacteria encode proteins that could potentially be involved in the degradation of pectin. The ability of representatives of Sphaerochaetaceae to use pectin for growth, as well as the evolutionary origin of genes encoding potential α-galacturonidase (GH4 family) and unsaturated glucuronyl/rhamnogalacturonyl hydrolase (GH105 family), involved in the degradation of pectin components, were studied.

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O. Yu. Troshina

Pushchino Scientific Center for Biological Research, Russian Academy of Sciences

Author for correspondence.
Email: oltro676@yandex.ru

Scryabin Institute of Biochemistry and Physiology of Microorganisms

Russian Federation, 142290, Pushchino

D. G. Naumoff

Research Centre of Biotechnology, Russian Academy of Sciences

Email: oltro676@yandex.ru

Winogradsky Institute of Microbiology

Russian Federation, 119071, Moscow

V. I. Rechkina

Pushchino Scientific Center for Biological Research, Russian Academy of Sciences

Email: oltro676@yandex.ru

Scryabin Institute of Biochemistry and Physiology of Microorganisms

Russian Federation, 142290, Pushchino

V. A. Shcherbakova

Pushchino Scientific Center for Biological Research, Russian Academy of Sciences

Email: oltro676@yandex.ru

Scryabin Institute of Biochemistry and Physiology of Microorganisms

Russian Federation, 142290, Pushchino

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3. Fig. 1 (a, b). Phylogenetic tree of proteins of the GH105 glycoside hydrolase family encoded in the genomes of Sphaerochaetaceae constructed by the maximum likelihood method: a ‒ the figure shows the phylogenetic position of the WP_244772448.1 protein from S. associata and its homologues; the analysis included 94 amino acid sequences; b ‒ the figure shows the position of the proteins WP_244773341.1, WP_244771860.1, WP_244773955.1 from S. associata and their homologues. The analysis included 74 amino acid sequences. Color legend for large taxa is indicated in the figure at the top left. Proteins with specific enzymatic activities, namely d-4,5-unsaturated rhamnogalacturonyl hydrolase (WP_014906487.1, WP_003243366.1, WP_011109152.1) and d-4,5-unsaturated α-galacturonidase (WP_008760990.1, WP_011107571.1, WP_123066362.1) are labeled. Bootstrap support values ​​≥50% are shown at branch points. The scale indicates the number of substitutions per amino acid sequence position. To simplify the display of trees, some clusters were collapsed into triangles with sides corresponding to the average branch length in a given cluster. The number of sequences is indicated next to the clusters. Sequence numbers and organisms in collapsed clusters are given in Table S3 (in order from top to bottom) in the Appendix.

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4. Fig. 2. Maximum-likelihood phylogenetic tree of potential GH4-family α-galacturonidases encoded in Sphaerochaetaceae genomes. The analysis included 67 protein sequences. Bootstrap values ​​≥50% are indicated at branch points. Scale bars indicate the number of substitutions per amino acid sequence position. Color legend for taxa is indicated in the figure at the top left. Proteins with α-galacturonidase activity WP_003244472.1 and WP_012995698.1 are labeled. To simplify the display of trees, some clusters have been collapsed into triangles with sides corresponding to the average branch length in a given cluster. Sequence counts are indicated next to the clusters. Sequence numbers and organisms in collapsed clusters are given in Table S3 in the Appendix.

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