Biofilms Program Innate Immunity for Persistence in

Overview

Journal Proc Natl Acad Sci U S A

Specialty Science

Date 2019 Jun 5

PMID 31160462

Citations 27

Authors

Stuti K Desai

Anup Padmanabhan

Sharvari Harshe

Ronen Zaidel-Bar

Linda J Kenney

Affiliations

Soon will be listed here.

Abstract

The adaptive in vivo mechanisms underlying the switch in lifestyles from the infectious form to a dormant form remain unknown. We employed as a heterologous host to understand the temporal dynamics of pathogenesis and to identify its lifestyle form in vivo. We discovered that exists as sessile aggregates, or in vivo biofilms, in the persistently infected gut. In the absence of in vivo biofilms, killed the host more rapidly by actively inhibiting innate immune pathways. Regulatory cross-talk between two major pathogenicity islands, SPI-1 and SPI-2, was responsible for biofilm-induced changes in host physiology during persistent infection. Thus, biofilm formation is a survival strategy in long-term infections, as prolonging host survival is beneficial for the parasitic lifestyle.

Citing Articles

Platforms for the Search for New Antimicrobial Agents Using In Vivo C. elegans Models.

Kalganova A, Eliseev I, Smirnov I, Terekhov S Acta Naturae. 2025; 16(4):15-26.

PMID: 39877009 PMC: 11771841. DOI: 10.32607/actanaturae.27348.

Nematode-bacteria interactions in bovine parasitic otitis.

Caracciolo M, Villela E, Machado L, Barreto M, Rosa A, Lopes-Torres E Rev Bras Parasitol Vet. 2025; 33(4):e019024.

PMID: 39774744 PMC: 11756828. DOI: 10.1590/S1984-29612024081.

A temporary cholesterol-rich diet and bacterial extracellular matrix factors favor spp. biofilm formation in the cecum.

Cruz-Cruz A, Schreeg M, Gunn J mBio. 2024; 16(1):e0324224.

PMID: 39636114 PMC: 11708031. DOI: 10.1128/mbio.03242-24.

biofilm formation diminishes bacterial proliferation in the intestine.

Thiers I, Lissens M, Langie H, Lories B, Steenackers H Biofilm. 2024; 8:100225.

PMID: 39469492 PMC: 11513601. DOI: 10.1016/j.bioflm.2024.100225.

The gut microbiota induces melanin deposits that act as substrates for -mediated aggregation of Typhimurium and enhance infection of the German cockroach vector.

Turner M, Van Hulzen L, Pietri J Microbiol Spectr. 2023; :e0211923.

PMID: 37606369 PMC: 10580948. DOI: 10.1128/spectrum.02119-23.

References

Costerton J, Stewart P, Greenberg E . Bacterial biofilms: a common cause of persistent infections. Science. 1999; 284(5418):1318-22. DOI: 10.1126/science.284.5418.1318. View

Lee A, Detweiler C, Falkow S . OmpR regulates the two-component system SsrA-ssrB in Salmonella pathogenicity island 2. J Bacteriol. 2000; 182(3):771-81. PMC: 94342. DOI: 10.1128/JB.182.3.771-781.2000. View

Singh P, Schaefer A, Parsek M, Moninger T, Welsh M, Greenberg E . Quorum-sensing signals indicate that cystic fibrosis lungs are infected with bacterial biofilms. Nature. 2000; 407(6805):762-4. DOI: 10.1038/35037627. View

Aballay A, Yorgey P, Ausubel F . Salmonella typhimurium proliferates and establishes a persistent infection in the intestine of Caenorhabditis elegans. Curr Biol. 2000; 10(23):1539-42. DOI: 10.1016/s0960-9822(00)00830-7. View

LABROUSSE A, Chauvet S, Couillault C, Kurz C, Ewbank J . Caenorhabditis elegans is a model host for Salmonella typhimurium. Curr Biol. 2000; 10(23):1543-5. DOI: 10.1016/s0960-9822(00)00833-2. View

Hodgkin J, Kuwabara P, Corneliussen B . A novel bacterial pathogen, Microbacterium nematophilum, induces morphological change in the nematode C. elegans. Curr Biol. 2001; 10(24):1615-8. DOI: 10.1016/s0960-9822(00)00867-8. View

Zogaj X, Nimtz M, Rohde M, Bokranz W, Romling U . The multicellular morphotypes of Salmonella typhimurium and Escherichia coli produce cellulose as the second component of the extracellular matrix. Mol Microbiol. 2001; 39(6):1452-63. DOI: 10.1046/j.1365-2958.2001.02337.x. View

Murli S, Watson R, Galan J . Role of tyrosine kinases and the tyrosine phosphatase SptP in the interaction of Salmonella with host cells. Cell Microbiol. 2001; 3(12):795-810. DOI: 10.1046/j.1462-5822.2001.00158.x. View

Feng X, Oropeza R, Kenney L . Dual regulation by phospho-OmpR of ssrA/B gene expression in Salmonella pathogenicity island 2. Mol Microbiol. 2003; 48(4):1131-43. DOI: 10.1046/j.1365-2958.2003.03502.x. View

10.

Tenor J, McCormick B, Ausubel F, Aballay A . Caenorhabditis elegans-based screen identifies Salmonella virulence factors required for conserved host-pathogen interactions. Curr Biol. 2004; 14(11):1018-24. DOI: 10.1016/j.cub.2004.05.050. View

11.

Feng X, Walthers D, Oropeza R, Kenney L . The response regulator SsrB activates transcription and binds to a region overlapping OmpR binding sites at Salmonella pathogenicity island 2. Mol Microbiol. 2004; 54(3):823-35. DOI: 10.1111/j.1365-2958.2004.04317.x. View

12.

Goodman A, Kulasekara B, Rietsch A, Boyd D, Smith R, Lory S . A signaling network reciprocally regulates genes associated with acute infection and chronic persistence in Pseudomonas aeruginosa. Dev Cell. 2004; 7(5):745-54. DOI: 10.1016/j.devcel.2004.08.020. View

13.

Ledeboer N, Jones B . Exopolysaccharide sugars contribute to biofilm formation by Salmonella enterica serovar typhimurium on HEp-2 cells and chicken intestinal epithelium. J Bacteriol. 2005; 187(9):3214-26. PMC: 1082824. DOI: 10.1128/JB.187.9.3214-3226.2005. View

14.

Faruque S, Biswas K, Udden S, Ahmad Q, Sack D, Nair G . Transmissibility of cholera: in vivo-formed biofilms and their relationship to infectivity and persistence in the environment. Proc Natl Acad Sci U S A. 2006; 103(16):6350-5. PMC: 1458881. DOI: 10.1073/pnas.0601277103. View

15.

Gibson D, White A, Snyder S, Martin S, Heiss C, Azadi P . Salmonella produces an O-antigen capsule regulated by AgfD and important for environmental persistence. J Bacteriol. 2006; 188(22):7722-30. PMC: 1636306. DOI: 10.1128/JB.00809-06. View

16.

Ellermeier J, Slauch J . Adaptation to the host environment: regulation of the SPI1 type III secretion system in Salmonella enterica serovar Typhimurium. Curr Opin Microbiol. 2007; 10(1):24-9. DOI: 10.1016/j.mib.2006.12.002. View

17.

Karlinsey J . lambda-Red genetic engineering in Salmonella enterica serovar Typhimurium. Methods Enzymol. 2007; 421:199-209. DOI: 10.1016/S0076-6879(06)21016-4. View

18.

Walthers D, Carroll R, Navarre W, Libby S, Fang F, Kenney L . The response regulator SsrB activates expression of diverse Salmonella pathogenicity island 2 promoters and counters silencing by the nucleoid-associated protein H-NS. Mol Microbiol. 2007; 65(2):477-93. DOI: 10.1111/j.1365-2958.2007.05800.x. View

19.

Irazoqui J, Urbach J, Ausubel F . Evolution of host innate defence: insights from Caenorhabditis elegans and primitive invertebrates. Nat Rev Immunol. 2009; 10(1):47-58. PMC: 2965059. DOI: 10.1038/nri2689. View

20.

Crawford R, Rosales-Reyes R, Ramirez-Aguilar M, Chapa-Azuela O, Alpuche-Aranda C, Gunn J . Gallstones play a significant role in Salmonella spp. gallbladder colonization and carriage. Proc Natl Acad Sci U S A. 2010; 107(9):4353-8. PMC: 2840110. DOI: 10.1073/pnas.1000862107. View