Transcriptome and Proteome of Fish-Pathogenic Streptococcus agalactiae Are Modulated by Temperature

Abstract

Streptococcus agalactiae is one of the most important pathogens associated with streptococcosis outbreaks in Nile tilapia farms worldwide. High water temperature (above 27°C) has been described as a predisposing factor for the disease in fish. At low temperatures (below 25°C), fish mortalities are not usually observed in farms. Temperature variation can modulate the expression of genes and proteins involved in metabolism, adaptation, and bacterial pathogenicity, thus increasing or decreasing the ability to infect the host. This study aimed to evaluate the transcriptome and proteome of a fish-pathogenic S. agalactiae strain SA53 subjected to in vitro growth at different temperatures using a microarray and label-free shotgun LC-HDMSE approach. Biological triplicates of isolates were cultured in BHIT broth at 22 or 32°C for RNA and protein isolation and submitted for transcriptomic and proteomic analyses. In total, 1,730 transcripts were identified in SA53, with 107 genes being differentially expressed between the temperatures evaluated. A higher number of genes related to metabolism, mainly from the phosphotransferase system (PTS) and ATP-binding cassette (ABC) transport system, were upregulated at 32°C. In the proteome analysis, 1,046 proteins were identified in SA53, of which 81 were differentially regulated between 22 and 32°C. Proteins involved in defense mechanisms, lipid transport and metabolism, and nucleotide transport and metabolism were upregulated at 32°C. A higher number of interactions were observed in proteins involved in nucleotide transport and metabolism. We observed a low correlation between the transcriptome and proteome datasets. Our study indicates that the transcriptome and proteome of a fish-adapted S. agalactiae strain are modulated by temperature, particularly showing differential expression of genes/proteins involved in metabolism, virulence factors, and adaptation.

Delineation of the pan-proteome of fish-pathogenic Streptococcus agalactiae strains using a label-free shotgun approach

“…However, our qualitative proteomic analysis of human- and fish-adapted GBS strains did not indicate the basis for the host specificity of the strains, as highly similar protein content was observed in all of the examined strains. A possible reason for the exclusive detection of these virulence proteins in fish-adapted GBS might be the temperature-independent regulation of several genes from this category on fish-adapted strains, as described in a recent study of our group [97]. Conversely, the strain NEM316 showed a distinct behavior of high expression of virulence genes at 40 °C when compared with low temperature conditions (i.e., 30 °C) [30].…”

Discovering the antibacterial mode of action of 3‐p‐trans‐coumaroyl‐2‐hydroxyquinic acid, a natural phenolic compound, against Staphylococcus aureus through an integrated transcriptomic and proteomic approach

“…In our integrative transcriptomic and proteomic analysis, a poor correlation was observed between the abundance of mRNA and proteins. Indeed, weak correlation between transcriptomic and proteomic profiles has been reported in other previous studies (Ahn, Gu, Koh, & Rice, 2017;Lv et al, 2017; Tavares et al, 2018). This is likely because complex posttranscriptional regulatory mechanisms, such as modification, processing, and translation, play a vital role in protein synthesis (Lv et al, 2017; Tavares et al, 2018).…”

“…After translation from mRNA, some proteins are secreted out of the bacterial cell and some proteins may be promptly degraded. The half‐life of mRNA in bacteria is short, while their corresponding proteins are more stable (Tavares et al, 2018). In addition, the technical limitations among the sample preparation, molecular identification, and bioinformatics analysis are responsible for a low correlation between mRNA and proteins abundance.…”

Cytotoxicity of Streptococcus agalactiae secretory protein on tilapia cultured cells

“…Bsp, PcsB and CAMP have been identified in various strains of S. agalactiae isolated from both fish and human (Li et al., 2016; Reinscheid et al., 2001; Tavares et al., 2018, 2019). The biological functions of these proteins in fish GSB strain have not been studied.…”

“…Tavares et al. (2018) reported the down‐regulation of cfb , but up‐regulation of CAMP factor in proteome analysis of S. agalactiae cultured at high temperature. In this study, CAMP factor was shown to up‐regulate at 32 and 37°C at both transcriptional and translational levels.…”