Abstract
ABSTRACTExtracellular polysaccharides are compounds secreted by microorganisms into the surrounding environment, and they are important for surface attachment and maintaining structural integrity within biofilms. The social nature of many extracellular polysaccharides remains unclear, and it has been suggested that they could function as either cooperative public goods or as traits that provide a competitive advantage. Here, we empirically tested the cooperative nature of the PSL polysaccharide, which is crucial for the formation of biofilms in Pseudomonas aeruginosa. We show that (i) PSL is not metabolically costly to produce; (ii) PSL provides population-level benefits in biofilms, for both growth and antibiotic tolerance; (iii) the benefits of PSL production are social and are shared with other cells; (iv) the benefits of PSL production appear to be preferentially directed toward cells which produce PSL; (v) cells which do not produce PSL are unable to successfully exploit cells which produce PSL. Taken together, this suggests that PSL is a social but relatively nonexploitable trait and that growth within biofilms selects for PSL-producing strains, even when multiple strains are on a patch (low relatedness at the patch level).
Highlights
Extracellular polysaccharides are compounds secreted by microorganisms into the surrounding environment, and they are important for surface attachment and maintaining structural integrity within biofilms
To ensure that our results are due to PSL production and not downstream c-di-GMP-dependent pleiotropic effects, we constitutively elevated c-diGMP in both our strains; we found that our results were c-di-GMP independent, because qualitatively identical results were recorded when we used non-wspF-mutated backgrounds (Fig. S2)
Influence on overall biofilm productivity (Fig. 2B); (vii) biofilms containing a higher proportion of PSLϩ cells are less susceptible to antibiotics (Fig. 4A); (viii) PSLϩ cells are better able to survive antibiotics than PSLϪ cells when growing in a mixed culture biofilm with PSLϪ cells (Fig. 4B); (ix) in a selection experiment, the relative success of PSLϩ versus PSLϪ cells was not influenced by relatedness at the patch level (Fig. 5)
Summary
Extracellular polysaccharides are compounds secreted by microorganisms into the surrounding environment, and they are important for surface attachment and maintaining structural integrity within biofilms. The first hypothesis assumes that the production of EPS provides a benefit to the local population of cells, which can be exploited by cells not producing EPS [5, 6] This is directly analogous to a range of public goods that have been studied in bacteria, such as iron-scavenging siderophore molecules and quorum sensing (QS) [7, 8]. Both theories and experiments have shown that the production of exploitable public goods is favored in spatially structured populations, which leads to a high relatedness between interacting cells, such that EPS producers tend to be aggregated and cooperate with other EPS producers [7,8,9]. EPS is not an exploitable (cooperative) public good; instead, it is a trait that provides an advantage in competition for resources
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