New insights into the relationship between Salmonella typhimurium and the German cockroach suggest biological mechanisms of vector-borne transmission

Diarrheal diseases are among the most common illnesses in the world and the bacterium Salmonella enterica serovar Typhimurium is a leading cause of morbidity and mortality from diarrhea globally. The German cockroach (Blattella germanica) has been linked to human outbreaks of S. Typhimurium, but the mechanisms of vector-borne transmission for this pathogen are not fully clear. Limited studies have suggested that bacterial pathogen transmission by cockroaches is mechanical. Towards the goal of obtaining novel insight into the mechanisms of S. Typhimurium transmission by cockroaches, here we orally provisioned wild-type and mutant strains of the bacteria to adult B. germanica and we examined various aspects of colonization and shedding. First, we demonstrate that S. Typhimurium undergoes replication at multiple phases during colonization of the cockroach gut. Second, we show the formation of biofilm-like aggregates by S. Typhimurium in the cockroach foregut. Lastly, we identify two mutant strains of S. Typhimurium that are deficient in colonization and shedding relative to isogenic controls, implicating type III secretion and the formation of fimbriae as two processes that are necessary for interaction with the cockroach vector. Our results suggest that transmission of S. Typhimurium by cockroaches is not entirely mechanical but may resemble biological transmission by other insect vectors which intake bacteria from infected hosts becoming subsequently colonized and enabling active transmission. This finding implicates cockroaches and their control as more important for public health than is currently appreciated. Additional studies to more precisely understand the cycle and biological mechanisms of vector-borne transmission are warranted.