Genome mining for peptidases in heat-tolerant and mesophilic fungi and putative adaptations for thermostability

Abstract

BackgroundPeptidases (EC 3.4) consist of a large group of hydrolytic enzymes that catalyze the hydrolysis of proteins accounting for approximately 65% of the total worldwide enzyme production. Peptidases from thermophilic fungi have adaptations to high temperature that makes them adequate for biotechnological application. In the present study, we profiled the genomes of heat-tolerant fungi and phylogenetically related mesophilic species for genes encoding for peptidases and their putative adaptations for thermostability.ResultsWe generated an extensive catalogue of these enzymes ranging from 241 to 820 peptidase genes in the genomes of 23 fungi. Thermophilic species presented the smallest number of peptidases encoding genes in relation to mesophilic species, and the peptidases families with a greater number of genes were the most affected. We observed differences in peptidases in thermophilic species in comparison to mesophilic counterparts, at (i) the genome level: a great reduction in the number of peptidases encoding genes that harbored a higher number of copies; (ii) in the primary protein structure: shifts in proportion of single or groups of amino acids; and (iii) in the three-dimensional structure: reduction in the number of internal cavities. Similar results were reported for extremely thermophilic proteins, but here we show for the first time that several changes also occurred on the moderate thermophilic enzymes of fungi. In regards to the amino acids composition, peptidases from thermophilic species in relation to the mesophilic ones, contained a larger proportion of Ala, Glu, Gly, Pro, Arg and Val residues and a lower number of Cys, His, Ile, Lys, Met, Asn, Gln, Ser, Thr and Trp residues (P < 0.05). Moreover, we observed an increase in the proportion of hydrophobic and charged amino acids and a decrease in polar amino acids.ConclusionsAlthough thermophilic fungi present less genes encoding for peptidases, these have adaptations that could play a role in thermal resistance from genome to protein structure level.Electronic supplementary materialThe online version of this article (10.1186/s12864-018-4549-5) contains supplementary material, which is available to authorized users.

An Overview of Genomics, Phylogenomics and Proteomics Approaches in Ascomycota

“…The presence of several DNA pathways related to mechanisms of thermal adaptation, in particular a ubiquitin degradation pathway was uncovered in analyzing the genome of Termomyces lanuginosus (Eurotiales; generally growing on dead woody material; [ 81 ]). Ubiquitin is known to play a crucial role in the responses to various stressors, such as nutrient limitation, heat shock, and heavy metal exposure and may be essential for T. lanuginosus to adapt during rising temperatures in composting materials [ 82 ]. Several mechanisms of DNA condensation machinery and repairing were also genome mined and they seem to make this fungus adapted to living at high temperatures [ 81 ].…”

“…More recently, de Oliveira et al [ 82 ] profiled the available genomes of all these thermophilic fungi and of their phylogenetically related mesophilic species for genes encoding for peptidases and their putative adaptations for thermal stability. Peptidase is one of the most important groups of industrial enzymes accounting for about 65% of the total enzyme production worldwide ([ 83 ] and references therein).…”

“…The authors generated an extensive catalogue of these enzymes ranging from 241 to 820 peptidase genes and found that thermophilic fungi have experienced a genome reduction in response to thermal adaptation, and consequently have lost also peptidases coding genes during their evolution. The authors [ 82 ] showed the largest reduction in the peptidase families with a higher number of genes, while those with fewer or single copies were less affected. The great amount of amino acid residues Ala, Glu, Gly, Pro, Arg and Val in peptidases from thermophilic fungi are in line with reports that some of these amino acids increase the thermal stability of the proteins [ 82 ].…”

“…The authors [ 82 ] showed the largest reduction in the peptidase families with a higher number of genes, while those with fewer or single copies were less affected. The great amount of amino acid residues Ala, Glu, Gly, Pro, Arg and Val in peptidases from thermophilic fungi are in line with reports that some of these amino acids increase the thermal stability of the proteins [ 82 ].…”

Disruption of a C69-Family Cysteine Dipeptidase Gene Enhances Heat Shock and UV-B Tolerances in Metarhizium acridum

“…In human fungal pathogens, secreted peptidase increased the fungal survival and virulence in Aspergillus fumigatus (Beauvais et al, 1997), Cryptococcus neoformans (Clarke et al, 2016) and Candida (Dutton et al, 2016). In thermophilic fungi, peptidases improved their adaptations to high temperature, providing them with adequacy for biotechnological application (de Oliveira et al, 2018).…”