Peeling back the many layers of competitive exclusion

Maurer, John J.; Cheng, Ying; Pedroso, Adriana; Thompson, Kasey K.; Akter, Shamima; Kwan, Tiffany; Morota, Gota; Kinstler, Sydney; Porwollik, Steffen; McClelland, Michael; Escalante-Semerena, Jorge C.; Lee, Margie D.

doi:10.3389/fmicb.2024.1342887

Title: Peeling back the many layers of competitive exclusion

Journal Article · Thu Mar 21 00:00:00 UTC 2024 · Frontiers in Microbiology

DOI: https://doi.org/10.3389/fmicb.2024.1342887 · OSTI ID:2530506

Maurer, John J. ^[1]; Cheng, Ying ^[2]; Pedroso, Adriana ^[2]; Thompson, Kasey K. ^[2]; Akter, Shamima ^[1]; Kwan, Tiffany ^[2]; Morota, Gota ^[1]; Kinstler, Sydney ^[1]; Porwollik, Steffen ^[3]; McClelland, Michael ^[3]; Escalante-Semerena, Jorge C. ^[2]; Lee, Margie D. ^[1]

Virginia Polytechnic Inst. and State Univ. (Virginia Tech), Blacksburg, VA (United States)
University of Georgia, Athens, GA (United States)
University of California, Irvine, CA (United States)

Baby chicks administered a fecal transplant from adult chickens are resistant to Salmonella colonization by competitive exclusion. A two-pronged approach was used to investigate the mechanism of this process. First, Salmonella response to an exclusive (Salmonella competitive exclusion product, Aviguard^®) or permissive microbial community (chicken cecal contents from colonized birds containing 7.85 Log₁₀Salmonella genomes/gram) was assessed ex vivo using a S. typhimurium reporter strain with fluorescent YFP and CFP gene fusions to rrn and hilA operon, respectively. Second, cecal transcriptome analysis was used to assess the cecal communities’ response to Salmonella in chickens with low (≤5.85 Log₁₀ genomes/g) or high (≥6.00 Log₁₀ genomes/g) Salmonella colonization. The ex vivo experiment revealed a reduction in Salmonella growth and hilA expression following co-culture with the exclusive community. The exclusive community also repressed Salmonella’s SPI-1 virulence genes and LPS modification, while the anti-virulence/inflammatory gene avrA was upregulated. Salmonella transcriptome analysis revealed significant metabolic disparities in Salmonella grown with the two different communities. Propanediol utilization and vitamin B12 synthesis were central to Salmonella metabolism co-cultured with either community, and mutations in propanediol and vitamin B12 metabolism altered Salmonella growth in the exclusive community. There were significant differences in the cecal community’s stress response to Salmonella colonization. Cecal community transcripts indicated that antimicrobials were central to the type of stress response detected in the low Salmonella abundance community, suggesting antagonism involved in Salmonella exclusion. This study indicates complex community interactions that modulate Salmonella metabolism and pathogenic behavior and reduce growth through antagonism may be key to exclusion.

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Research Organization:: Univ. of Georgia, Athens, GA (United States); University of Georgia, Athens, GA (United States)

Sponsoring Organization:: National Institutes of Health (NIH); USDOE Office of Science (SC), Basic Energy Sciences (BES). Chemical Sciences, Geosciences & Biosciences Division (CSGB)

Grant/Contract Number:: SC0015662

OSTI ID:: 2530506

Journal Information:: Frontiers in Microbiology, Journal Name: Frontiers in Microbiology Vol. 15; ISSN 1664-302X

Publisher:: Frontiers Research FoundationCopyright Statement

Country of Publication:: United States

Language:: English

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