Clinically relevant pathogens on surfaces display differences in survival and transcriptomic response in relation to probiotic and traditional cleaning strategies

Abstract

Indoor surfaces are paradoxically presumed to be both colonized by pathogens, necessitating disinfection, and “microbial wastelands.” In these resource-poor, dry environments, competition and decay are thought to be important drivers of microbial community composition. However, the relative contributions of these two processes have not been specifically evaluated. To bridge this knowledge gap, we used microcosms to evaluate whether interspecies interactions occur on surfaces. We combined transcriptomics and traditional microbiology techniques to investigate whether competition occurred between two clinically important pathogens, Acinetobacter baumannii and Klebsiella pneumoniae, and a probiotic cleaner containing a consortium of Bacillus species. Probiotic cleaning seeks to take advantage of ecological principles such as competitive exclusion, thus using benign microorganisms to inhibit viable pathogens, but there is limited evidence that competitive exclusion in fact occurs in environments of interest (i.e., indoor surfaces). Our results indicate that competition in this setting has a negligible impact on community composition but may influence the functions expressed by active organisms. Although Bacillus spp. remained viable on surfaces for an extended period of time after application, viable colony forming units (CFUs) of A. baumannii recovered following exposure to a chemical-based detergent with and without Bacillus spp. showed no statistical difference. Similarly, for K. pneumoniae, there were small statistical differences in CFUs between cleaning scenarios with or without Bacillus spp. in the chemical-based detergent. The transcriptome of A. baumannii with and without Bacillus spp. exposure shared a high degree of similarity in overall gene expression, but the transcriptome of K. pneumoniae differed in overall gene expression, including reduced response in genes related to antimicrobial resistance. Together, these results highlight the need to fully understand the underlying biological and ecological mechanisms for community assembly and function on indoor surfaces, as well as having practical implications for cleaning and disinfection strategies for infection prevention.

Biocontrol in built environments to reduce pathogen exposure and infection risk

“…2 ; [ 94 ]), although the effectiveness of these compounds has not specifically been demonstrated in the built environment. Several studies have demonstrated that Bacillus intervention enhances the pathogen exclusion properties of the extant surface microbiome [ 95 , 96 ]. However, the lack of a defined mechanism of action behind such biocontrol suggests an urgent need to perform new studies aimed at elucidating these modalities.…”

“…To test the activity of these spore sprays, a commercially available cleaner containing either Bacillus spp. spores or a spore-free version of the cleaner was applied to steel coupons; then, the coupons were inoculated with either Acinetobacter baumannii or K. pneumoniae [ 95 ]. The coupons were sampled at 3, 24, and 72 hours for colony-forming unit (CFU) enumeration to determine whether the presence of the cleaner, with or without Bacillus spores, decreased the survival rate of the pathogens compared to cleaner-free controls [ 95 ].…”

“…spores or a spore-free version of the cleaner was applied to steel coupons; then, the coupons were inoculated with either Acinetobacter baumannii or K. pneumoniae [ 95 ]. The coupons were sampled at 3, 24, and 72 hours for colony-forming unit (CFU) enumeration to determine whether the presence of the cleaner, with or without Bacillus spores, decreased the survival rate of the pathogens compared to cleaner-free controls [ 95 ]. However, there was no significant difference in A. baumannii survival rates in the presence or absence of the cleaner, with or without Bacillus .…”

“…These lab-based studies shed light on how Bacillus , the primary biocontrol bacteria used in commercial probiotic cleaning products, behaves in different environments and varied microbial communities. However, some lab studies show that Bacillus mostly fails to germinate and has a limited impact on the survival of pathogens like A. baumannii and K. pneumoniae [ 95 ]. Conversely, using a probiotic cleaner appears to establish a microbial ecosystem that effectively kills or inhibits pathogens, but that cleaning with soap also leads to a microbial community that is just as effective at pathogen inhibition [ 96 ].…”

Persistence of microbiological hazards in food and feed production and processing environments

“…A high adaptive capacity against physical–chemical factors as well as biofilm‐forming capacity could partly explain the persistence phenomenon (EFSA BIOHAZ Panel, 2018). Recent advances in next generation sequencing technologies have promoted a more detailed characterisation of persistent isolates through whole genome sequencing (WGS) and transcriptomics, and offer opportunities for the study of persistence episodes at processing plant level through the characterisation of the FFPE microbiome through metagenomics, which will provide information on the role of complex microbial communities and the cellular processes and microbial interactions driving microbial persistence in the FFPE (Fenner et al., 2021; Hu et al., 2022).…”