Contrasted evolutionary constraints on carbohydrate active enzymes (CAZymes) in selected Frankia strains
Abstract
Carbohydrate active enzymes (CAZymes) are capable of breaking complex polysaccharides into simpler form. In plant-host-associated microorganisms CAZymes are known to be involved in plant cell wall degradation. However, the biology and evolution of Frankia CAZymes are largely unknown. In the present study, we took a genomic approach to evaluate the presence and putative roles of CAZymes in Frankia. The CAZymes were found to be potentially highly expressed (PHX) proteins and contained more aromatic amino acids, which increased their biosynthetic energy cost. These energy rich amino acids were present in the active sites of CAZymes aiding in their carbohydrate binding capacity. Phylogenetic and evolutionary analyses showed that, in Frankia strains with the capacity to nodulate host plants, CAZymes were evolving slower than the other PHX genes, whereas similar genes from non-nodulating (or ineffectively nodulating) Frankia strains showed little variation in their evolutionary constraints compared to other PHX genes. Thus, the present study revealed the persistence of a strong purifying selection on CAZymes of Frankia indicating their crucial role.
Keywords
Carbohydrate active enzymes Frankia Nodulation Codon usage Amino acid usage Comparative genomics Evolution PhylogenyNotes
Authors contribution
Indrani Sarkar conceived the idea. Arnab Sen and Indrani Sarkar designed the study, performed research. Arnab Sen, Louis S. Tisa, Maher Gtari and Indrani Sarkar analysed data. All the authors wrote the paper and approved.
Funding
IS acknowledges UGC-BSR senior research fellowship, Govt, of India. AS is thankful to DBT Govt. of India for Bioinformatics Facility, University of North Bengal. LST was supported by the USDA National Institute of Food and Agriculture Hatch 022821.
Compliance with ethical standards
Conflict of interest
The authors declare that they have no conflict of interest.
Ethical approval
This article does not contain any studies with human participants or animals performed by anyof the authors.
Supplementary material
References
- Andrade AC, Fróes A, Lopes FÁC, Thompson FL, Krüger RH, Dinsdale E, Bruce T (2017) Diversity of microbial carbohydrate-active enzymes (CAZymes) associated with freshwater and soil samples from caatinga biome. Microbialecology 74(1):89–105Google Scholar
- André I, Potocki-Véronèse G, Barbe S, Moulis C, Remaud-Siméon M (2014) CAZyme discovery and design for sweet dreams. Curr Opin Chem Biol 19:17–24CrossRefGoogle Scholar
- Cantarel BL, Coutinho PM, Rancurel C, Bernard T, Lombard V, Henrissat B (2008) The carbohydrate-active EnZymes database (CAZy): an expert resource for glycogenomics. Nucleic Acids Res 37:D233–D238CrossRefGoogle Scholar
- Ghodhbane-Gtari F, Nouioui I, Boudabous A, Gtari M (2010) 16S–23S rRNAintergenic spacer region variability in the genus Frankia. Microb Ecol 60(3):487–495CrossRefGoogle Scholar
- Gibson AH (1966) The carbohydrate requirements for symbiotic nitrogen fixation: a” whole-plant” growth analysis approach. Aust J Biol Sci 19(4):499–516CrossRefGoogle Scholar
- Goris J, Konstantinidis KT, Klappenbach JA, Coenye T, Vandamme P, Tiedje JM (2007) DNA–DNA hybridization values and their relationship to whole-genome sequence similarities. Int J Syst Evol Microbiol 57(1):81–91CrossRefGoogle Scholar
- López-Mondéjar R, Zühlke D, Becher D, Riedel K, Baldrian P (2016) Cellulose and hemicellulose decomposition by forest soil bacteria proceeds by the action of structurally variable enzymatic systems. Sci Rep 29(6):25279CrossRefGoogle Scholar
- Normand P, Benson DR, Berry AM, Tisa LS (2014) The family frankiaceae. In: The prokaryotes. Springer, Berlin, pp 339–356Google Scholar
- Peden J (1997) CodonW. Trinity College, DublinGoogle Scholar
- Roy A, Mukhopadhyay S, Sarkar I, Sen A (2015) Comparative investigation of the various determinants that influence the codon and amino acid usage patterns in the genus Bifidobacterium. World J Microbiol Biotechnol 31(6):959–981CrossRefGoogle Scholar
- Sarkar I, Tisa LS, Gtari M, Sen A (2018) Biosynthetic energy cost of potentially highly expressed proteins vary with niche in selected actinobacteria. J Basic Microbiol 58(2):154–161CrossRefGoogle Scholar
- Sen A, Daubin V, Abrouk D, Gifford I, Berry AM, Normand P (2014) Phylogeny of the class Actinobacteria revisited in the light of complete genomes. The orders ‘Frankiales’ and Micrococcales should be split into coherent entities: proposal of Frankiales ord. nov., Geodermatophilales ord. nov., Acidothermales ord. nov. and Nakamurellales ord. nov. Int J Syst Evol Microbiol 64:3821–3832CrossRefGoogle Scholar
- Sharp PM, Li WH (1987) The codon adaptation index—a measure of directional synonymous codon usage bias, and its potential applications. Nucleic Acids Res 15(3):1281–1295CrossRefGoogle Scholar
- Simonet P, Normand P, Hirsch AM, Akkermans AD (1990) The genetics of the Frankia-actinorhizal symbiosis. In: Molecular biology of symbiotic nitrogen fixation, pp 77–109Google Scholar
- Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24(8):1596–1599CrossRefGoogle Scholar
- Tasse L, Bercovici J, Pizzut-Serin S, Robe P, Tap J, Klopp C, Cantarel BL, Coutinho PM, Henrissat B, Leclerc M, Doré J (2010) Functional metagenomics to mine the human gut microbiome for dietary fiber catabolic enzymes. Genome Res 20(11):1605–1612CrossRefGoogle Scholar
- Tatusov RL, Fedorova ND, Jackson JD, Jacobs AR, Kiryutin B, Koonin EV, Krylov DM, Mazumder R, Mekhedov SL, Nikolskaya AN, Rao BS (2003) The COG database: an updated version includes eukaryotes. BMC Bioinform 4(1):41CrossRefGoogle Scholar
- Tisa LS, Oshone R, Sarkar I, Ktari A, Sen A, Gtari M (2016) Genomic approaches toward understanding the actinorhizal symbiosis: an update on the status of the Frankia genomes. Symbiosis 70(1–3):5–16CrossRefGoogle Scholar
- Vesth T, Lagesen K, Acar Ö, Ussery D (2013) CMG-biotools, a free workbench for basic comparative microbial genomics. PLoS ONE 8(4):e60120CrossRefGoogle Scholar
- Vorwerk S, Somerville S, Somerville C (2004) The role of plant cell wall polysaccharide composition in disease resistance. Trends Plant Sci 9(4):203–209CrossRefGoogle Scholar
- Xia X, Xie Z (2001) DAMBE: software package for data analysis in molecular biology and evolution. J Hered 92(4):371–373CrossRefGoogle Scholar
- Yin Y, Mao X, Yang J, Chen X, Mao F, Xu Y (2012) dbCAN: a web resource for automated carbohydrate-active enzyme annotation. Nucleic Acids Res 40(1):W445–W451CrossRefGoogle Scholar
- Zerillo MM, Adhikari BN, Hamilton JP, Buell CR, Lévesque CA, Tisserat N (2013) Carbohydrate-active enzymes in Pythium and their role in plant cell wall and storage polysaccharide degradation. PLoS ONE 8(9):e72572CrossRefGoogle Scholar