Dataset Information

Multicellular String-Like Structure Formation by Salmonella Typhimurium Depends on Cellulose Production: Roles of Diguanylate Cyclases, YedQ and YfiN.

ABSTRACT: Bacteria face diverse stresses in the environment and, sometimes, respond by forming multi-cellular structures, e.g., biofilms. Here, we report a novel macroscopic and multi-cellular structure formed by Salmonella Typhimurium, which resembles small strings. These string-like structures, ?1 cm long, are induced under some stress conditions: iron deprivation by 2,2-Bipyridyl or low amounts of antibiotics or ethanol in minimal media. However, cells in strings revert back to planktonic growth upon return to nutrient rich media. Compared to planktonic cells, strings are more resistant to antibiotics and oxidative stress. Also, strains lacking csgD or rpoS, which are defective in the classical rdar biofilm formation, form strings. Furthermore, some biofilm inducing conditions do not result in strings and vice-versa, demonstrating that strings are not related to classical CsgD-dependent biofilms. Cells in a string are held together by cellulose and a strain lacking bcsA, which is defective in cellulose production, does not form strings. In addition, reductive stress conditions such as dithiothreitol (DTT) or mutations in the Disulfide bonding system (DSB) also give rise to strings. The amounts of c-di-GMP are increased upon string formation and studies with single and double deletion strains of the diguanylate cyclases, yedQ (STM1987) primarily and yfiN (STM2672) partly, revealed their importance for string formation. This is the first study showcasing the ability of Salmonella to produce high amounts of cellulose in liquid culture, instead of an interface, in a CsgD-independent manner. The relevance and possible applications of strings in the production of bacterial cellulose and bioremediation are discussed.

SUBMITTER: Varghese A

PROVIDER: S-EPMC7769011 | biostudies-literature | 2020

REPOSITORIES: biostudies-literature

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Multicellular String-Like Structure Formation by <i>Salmonella</i> Typhimurium Depends on Cellulose Production: Roles of Diguanylate Cyclases, YedQ and YfiN.

Varghese Alan A Ray Semanti S Verma Taru T Nandi Dipankar D

Frontiers in microbiology 20201214

Bacteria face diverse stresses in the environment and, sometimes, respond by forming multi-cellular structures, e.g., biofilms. Here, we report a novel macroscopic and multi-cellular structure formed by <i>Salmonella</i> Typhimurium, which resembles small strings. These string-like structures, ∼1 cm long, are induced under some stress conditions: iron deprivation by 2,2-Bipyridyl or low amounts of antibiotics or ethanol in minimal media. However, cells in strings revert back to planktonic growth ...[more]

PMID: 33381103

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Project description:UnlabelledNontyphoidal Salmonella enterica serovar Typhimurium is a frequent cause of bloodstream infections in children and HIV-infected adults in sub-Saharan Africa. Most isolates from African patients with bacteremia belong to a single sequence type, ST313, which is genetically distinct from gastroenteritis-associated ST19 strains, such as 14028s and SL1344. Some studies suggest that the rapid spread of ST313 across sub-Saharan Africa has been facilitated by anthroponotic (person-to-person) transmission, eliminating the need for Salmonella survival outside the host. While these studies have not ruled out zoonotic or other means of transmission, the anthroponotic hypothesis is supported by evidence of extensive genomic decay, a hallmark of host adaptation, in the sequenced ST313 strain D23580. We have identified and demonstrated 2 loss-of-function mutations in D23580, not present in the ST19 strain 14028s, that impair multicellular stress resistance associated with survival outside the host. These mutations result in inactivation of the KatE stationary-phase catalase that protects high-density bacterial communities from oxidative stress and the BcsG cellulose biosynthetic enzyme required for the RDAR (red, dry, and rough) colonial phenotype. However, we found that like 14028s, D23580 is able to elicit an acute inflammatory response and cause enteritis in mice and rhesus macaque monkeys. Collectively, these observations suggest that African S. Typhimurium ST313 strain D23580 is becoming adapted to an anthroponotic mode of transmission while retaining the ability to infect and cause enteritis in multiple host species.ImportanceThe last 3 decades have witnessed an epidemic of invasive nontyphoidal Salmonella infections in sub-Saharan Africa. Genomic analysis and clinical observations suggest that the Salmonella strains responsible for these infections are evolving to become more typhoid-like with regard to patterns of transmission and virulence. This study shows that a prototypical African nontyphoidal Salmonella strain has lost traits required for environmental stress resistance, consistent with an adaptation to a human-to-human mode of transmission. However, in contrast to predictions, the strain remains capable of causing acute inflammation in the mammalian intestine. This suggests that the systemic clinical presentation of invasive nontyphoidal Salmonella infections in Africa reflects the immune status of infected hosts rather than intrinsic differences in the virulence of African Salmonella strains. Our study provides important new insights into the evolution of host adaptation in bacterial pathogens.

Project description:BACKGROUND: Bacteria employ complex transcriptional networks involving multiple genes in response to stress, which is not limited to gene and protein networks but now includes small RNAs (sRNAs). These regulatory RNA molecules are increasingly shown to be able to initiate regulatory cascades and modulate the expression of multiple genes that are involved in or required for survival under environmental challenge. Despite mounting evidence for the importance of sRNAs in stress response, their role upon antibiotic exposure remains unknown. In this study, we sought to determine firstly, whether differential expression of sRNAs occurs upon antibiotic exposure and secondly, whether these sRNAs could be attributed to microbial tolerance to antibiotics. RESULTS: A small scale sRNA cloning strategy of Salmonella enterica serovar Typhimurium SL1344 challenged with half the minimal inhibitory concentration of tigecycline identified four sRNAs (sYJ5, sYJ20, sYJ75 and sYJ118) which were reproducibly upregulated in the presence of either tigecycline or tetracycline. The coding sequences of the four sRNAs were found to be conserved across a number of species. Genome analysis found that sYJ5 and sYJ118 mapped between the 16S and 23S rRNA encoding genes. sYJ20 (also known as SroA) is encoded upstream of the tbpAyabKyabJ operon and is classed as a riboswitch, whilst its role in antibiotic stress-response appears independent of its riboswitch function. sYJ75 is encoded between genes that are involved in enterobactin transport and metabolism. Additionally we find that the genetic deletion of sYJ20 rendered a reduced viability phenotype in the presence of tigecycline, which was recovered when complemented. The upregulation of some of these sRNAs were also observed when S. Typhimurium was challenged by ampicillin (sYJ5, 75 and 118); or when Klebsiella pneumoniae was challenged by tigecycline (sYJ20 and 118). CONCLUSIONS: Small RNAs are overexpressed as a result of antibiotic exposure in S. Typhimurium where the same molecules are upregulated in a related species or after exposure to different antibiotics. sYJ20, a riboswitch, appears to possess a trans-regulatory sRNA role in antibiotic tolerance. These findings imply that the sRNA mediated response is a component of the bacterial response to antibiotic challenge.

Dataset Information

Multicellular String-Like Structure Formation by Salmonella Typhimurium Depends on Cellulose Production: Roles of Diguanylate Cyclases, YedQ and YfiN.

Publications

Multicellular String-Like Structure Formation by <i>Salmonella</i> Typhimurium Depends on Cellulose Production: Roles of Diguanylate Cyclases, YedQ and YfiN.

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