1887

Abstract

Integrons are genetic platforms that capture, rearrange and express mobile modules called gene cassettes. The best characterized gene cassettes encode antibiotic resistance, but the function of most integron gene cassettes remains unknown. Functional predictions suggest that many gene cassettes could encode proteins that facilitate interactions with other cells and with the extracellular environment. Because cell interactions are essential for biofilm stability, we sequenced gene cassettes from biofilms growing on the surface of the marine macroalgae and . Algal samples were obtained from coastal rock platforms around Sydney, Australia, using seawater as a control. We demonstrated that integrons in microbial biofilms did not sample genes randomly from the surrounding seawater, but harboured specific functions that potentially provided an adaptive advantage to both the bacterial cells in biofilm communities and their macroalgal host. Further, integron gene cassettes had a well-defined spatial distribution, suggesting that each bacterial biofilm acquired these genetic elements via sampling from a large but localized pool of gene cassettes. These findings suggest two forms of filtering: a selective acquisition of different integron-containing bacterial species into the distinct biofilms on and surfaces, and a selective retention of unique populations of gene cassettes at each sampling location.

  • This is an open-access article distributed under the terms of the Creative Commons Attribution License. This article was made open access via a Publish and Read agreement between the Microbiology Society and the corresponding author’s institution.
Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.001446
2024-03-15
2024-04-22
Loading full text...

Full text loading...

/deliver/fulltext/micro/170/3/mic001446.html?itemId=/content/journal/micro/10.1099/mic.0.001446&mimeType=html&fmt=ahah

References

  1. Ghaly TM, Gillings MR, Penesyan A, Qi Q, Rajabal V et al. The natural history of integrons. Microorganisms 2021; 9:2212 [View Article] [PubMed]
    [Google Scholar]
  2. Recchia GD, Hall RM. Gene cassettes: a new class of mobile element. Microbiology 1995; 141:3015–3027 [View Article] [PubMed]
    [Google Scholar]
  3. Ghaly TM, Geoghegan JL, Tetu SG, Gillings MR. The peril and promise of integrons: beyond antibiotic resistance. Trends Microbiol 2020; 28:455–464 [View Article] [PubMed]
    [Google Scholar]
  4. Ghaly TM, Geoghegan JL, Alroy J, Gillings MR. High diversity and rapid spatial turnover of integron gene cassettes in soil. Environ Microbiol 2019; 21:1567–1574 [View Article] [PubMed]
    [Google Scholar]
  5. Grossart HP. Ecological consequences of bacterioplankton lifestyles: changes in concepts are needed. Environ Microbiol Rep 2010; 2:706–714 [View Article] [PubMed]
    [Google Scholar]
  6. Roth-Schulze AJ, Pintado J, Zozaya-Valdés E, Cremades J, Ruiz P et al. Functional biogeography and host specificity of bacterial communities associated with the marine green alga Ulva spp. Mol Ecol 2018; 27:1952–1965 [View Article] [PubMed]
    [Google Scholar]
  7. Rao D, Skovhus T, Tujula N, Holmström C, Dahllöf I et al. Ability of Pseudoalteromonas tunicata to colonize natural biofilms and its effect on microbial community structure. FEMS Microbiol Ecol 2010; 73:450–457 [View Article] [PubMed]
    [Google Scholar]
  8. Penesyan A, Marshall-Jones Z, Holmstrom C, Kjelleberg S, Egan S. Antimicrobial activity observed among cultured marine epiphytic bacteria reflects their potential as a source of new drugs. FEMS Microbiol Ecol 2009; 69:113–124 [View Article] [PubMed]
    [Google Scholar]
  9. Penesyan A, Tebben J, Lee M, Thomas T, Kjelleberg S et al. Identification of the antibacterial compound produced by the marine epiphytic bacterium Pseudovibrio sp. D323 and related sponge-associated bacteria. Mar Drugs 2011; 9:1391–1402 [View Article] [PubMed]
    [Google Scholar]
  10. Gillings MR. Rapid extraction of PCR-competent DNA from recalcitrant environmental samples. Methods Mol Biol 2014; 1096:17–23 [View Article] [PubMed]
    [Google Scholar]
  11. Stokes HW, Holmes AJ, Nield BS, Holley MP, Nevalainen KM et al. Gene cassette PCR: sequence-independent recovery of entire genes from environmental DNA. Appl Environ Microbiol 2001; 67:5240–5246 [View Article] [PubMed]
    [Google Scholar]
  12. Schwarze K, Buchanan J, Fermont JM, Dreau H, Tilley MW et al. The complete costs of genome sequencing: a microcosting study in cancer and rare diseases from a single center in the United Kingdom. Genet Med 2020; 22:85–94 [View Article] [PubMed]
    [Google Scholar]
  13. Ghaly TM, Penesyan A, Pritchard A, Qi Q, Rajabal V et al. Methods for the targeted sequencing and analysis of integrons and their gene cassettes from complex microbial communities. Microb Genom 2022; 8:000788 [View Article] [PubMed]
    [Google Scholar]
  14. Hyatt D, Chen G-L, Locascio PF, Land ML, Larimer FW et al. Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC Bioinformatics 2010; 11:119 [View Article] [PubMed]
    [Google Scholar]
  15. Balaji A, Kille B, Kappell AD, Godbold GD, Diep M et al. SeqScreen: accurate and sensitive functional screening of pathogenic sequences via ensemble learning. Genome Biol 2022; 23:133 [View Article] [PubMed]
    [Google Scholar]
  16. Armenteros JJA, Tsirigos KD, Sønderby CK, Petersen TN, Winther O et al. SignalP 5.0 improves signal peptide predictions using deep neural networks. Nat Biotechnol 2019; 37:420–423 [View Article] [PubMed]
    [Google Scholar]
  17. Ghaly TM, Tetu SG, Gillings MR. Predicting the taxonomic and environmental sources of integron gene cassettes using structural and sequence homology of attC sites. Commun Biol 2021; 4:946 [View Article] [PubMed]
    [Google Scholar]
  18. Gillings MR. Class 1 integrons as invasive species. Curr Opin Microbiol 2017; 38:10–15 [View Article] [PubMed]
    [Google Scholar]
  19. Gillings MR. Integrons: past, present, and future. Microbiol Mol Biol Rev 2014; 78:257–277 [View Article] [PubMed]
    [Google Scholar]
  20. Koenig JE, Boucher Y, Charlebois RL, Nesbø C, Zhaxybayeva O et al. Integron-associated gene cassettes in Halifax harbour: assessment of a mobile gene pool in marine sediments. Environ Microbiol 2008; 10:1024–1038 [View Article] [PubMed]
    [Google Scholar]
  21. Rowe-Magnus DA, Guerout AM, Biskri L, Bouige P, Mazel D. Comparative analysis of superintegrons: engineering extensive genetic diversity in the Vibrionaceae. Genome Res 2003; 13:428–442 [View Article] [PubMed]
    [Google Scholar]
  22. Boucher Y, Labbate M, Koenig JE, Stokes HW. Integrons: mobilizable platforms that promote genetic diversity in bacteria. Trends Microbiol 2007; 15:301–309 [View Article] [PubMed]
    [Google Scholar]
  23. Mekinić I, Skroza D, Šimat V, Hamed I, Čagalj M et al. Phenolic content of brown algae (Pheophyceae) species: extraction, identification, and quantification. Biomolecules 2019; 9:244 [View Article] [PubMed]
    [Google Scholar]
  24. Rao D, Webb JS, Kjelleberg S. Microbial colonization and competition on the marine alga Ulva australis. Appl Environ Microbiol 2006; 72:5547–5555 [View Article] [PubMed]
    [Google Scholar]
  25. Burke C, Thomas T, Lewis M, Steinberg P, Kjelleberg S. Composition, uniqueness and variability of the epiphytic bacterial community of the green alga Ulva australis. ISME J 2011; 5:590–600 [View Article] [PubMed]
    [Google Scholar]
  26. Burke C, Steinberg P, Rusch D, Kjelleberg S, Thomas T. Bacterial community assembly based on functional genes rather than species. Proc Natl Acad Sci U S A 2011; 108:14288–14293 [View Article] [PubMed]
    [Google Scholar]
  27. Burke C. A metagenomic analysis of the epiphytic bacterial community from the green macroalga. Ulva australis 2010
    [Google Scholar]
  28. Amarasiri M, Sano D, Suzuki S. Understanding human health risks caused by antibiotic resistant bacteria (ARB) and antibiotic resistance genes (ARG) in water environments: current knowledge and questions to be answered. Cri Review Envir Sci Technol 2020; 50:2016–2059 [View Article]
    [Google Scholar]
  29. Flores-Vargas G, Bergsveinson J, Lawrence JR, Korber DR. Environmental biofilms as reservoirs for antimicrobial resistance. Front Microbiol 2021; 12:766242 [View Article] [PubMed]
    [Google Scholar]
  30. Ghaly TM, Paulsen IT, Sajjad A, Tetu SG, Gillings MR. A novel family of Acinetobacter mega-plasmids are disseminating multi-drug resistance across the globe while acquiring location-specific accessory genes. Front Microbiol 2020; 11:605952 [View Article] [PubMed]
    [Google Scholar]
  31. Partridge SR, Tsafnat G, Coiera E, Iredell JR. Gene cassettes and cassette arrays in mobile resistance integrons. FEMS Microbiol Rev 2009; 33:757–784 [View Article] [PubMed]
    [Google Scholar]
  32. Tansirichaiya S, Rahman MA, Antepowicz A, Mullany P, Roberts AP. Detection of novel integrons in the metagenome of human saliva. PLoS One 2016; 11:e0157605 [View Article] [PubMed]
    [Google Scholar]
  33. Wang Z, Chen Q, Zhang J, Guan T, Chen Y et al. Critical roles of cyanobacteria as reservoir and source for antibiotic resistance genes. Environ Int 2020; 144:106034 [View Article] [PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.001446
Loading
/content/journal/micro/10.1099/mic.0.001446
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error