Abstract

At low temperatures, psychrotolerant B. cereus group strains exhibit a higher growth rate than mesophilic strains do. However, the different survival responses of the psychrotolerant strain (BCG34) and the mesophilic strain (BCGT) at low temperatures are unclear. We investigated the morphological and genomic features of BCGT and BCG34 to characterize their growth strategies at low temperatures. At low temperatures, morphological changes were observed only in BCGT. These morphological changes included the elongation of rod-shaped cells, whereas the cell shape in BCG34 was unchanged at the low temperature. A transcriptomic analysis revealed that both species exhibited different growth-related traits during low-temperature growth. The BCGT strain induces fatty acid biosynthesis, sulfur assimilation, and methionine and cysteine biosynthesis as a survival mechanism in cold systems. Increases in energy metabolism and fatty acid biosynthesis in the mesophilic B. cereus group strain might explain its ability to grow at low temperatures. Several pathways involved in carbohydrate mechanisms were downregulated to conserve the energy required for growth. Peptidoglycan biosynthesis was upregulated, implying that a change of gene expression in both RNA-Seq and RT-qPCR contributed to sustaining its growth and rod shape at low temperatures. These results improve our understanding of the growth response of the B. cereus group, including psychrotolerant B. cereus group strains, at low temperatures and provide information for improving bacterial inhibition strategies in the food industry.

Highlights

  • Our results suggest that increases in genes related to sulfur assimilation metabolism and cysteine biosynthesis might ensure bacterial survival during the growth of mesophilic B. cereus group strains at low temperatures

  • This strategy might not be appropriate for inhibiting the growth of psychrotolerant B. cereus group strains because these strains are able to survive with a high growth rate under cold conditions

  • Understanding of the mechanisms associated with bacterial growth at low temperatures is needed to improve the systems used for the management of food safety by inhibiting the frequency of B. cereus group proliferation in foodstuffs distributed via cold supply chains

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Summary

Introduction with regard to jurisdictional claims in

The Bacillus cereus group comprises more than 20 species with close genetic similarity and nine species, namely, B. anthracis, B. cereus, B. cytotoxicus, B. mycoides, B. pseudomycoides, B. thuringiensis, B. toyonensis, B. weihenstephanensis, and B. wiedmannii that can cause anthrax or foodborne illness in humans or insects [1,2,3] depending on the presence and expression of virulence genes. Microorganisms 2021, 9, 1255 that is favorable for bacterial survival and the growth of psychrotolerant B. cereus strains. The growth of B. cereus at low temperatures is associated with a higher proportion of unsaturated fatty acids in the bacterial membrane than that found at optimal growth temperatures [13]. B. cereus group is not traditionally considered a psychrotrophic species, but psychrotolerant B. cereus group strains possess a growth ability at below 10 ◦ C and have successfully colonized at low temperatures without cold adaptation. We investigated whether a psychrotolerant B. cereus group strain reveals a similar response to growth at low temperatures as a mesophilic B. cereus group strain. The present study may provide a better understanding of the bacterial growth response employed by B. cereus group strains, including psychrotolerant strains, at low temperatures

Bacterial Strains and Growth Conditions
Bacterial Growth Capability at Low Temperature
Cell Lysis and RNA Isolation
Illumina Sequencing
Differential Gene Expression Analysis
Statistical Analyses
Results
Growth of mesophilic
Microscopic
Differential Expression Analysis of Cold-Response-Related Genes
Lipid Metabolism
Energy Metabolism
Amino Acid Metabolism
Carbohydrate Metabolism
Conclusions
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