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Memorial University of Newfoundland, St. John’s, Newfoundland and Labrador, CanadaK. K. S. Layton & P. V. R. SnelgroveFisheries and Oceans Canada, St. John’s, Newfoundland and Labrador, CanadaK. K. S. Layton, J. B. Dempson, T. Kess, S. J. Lehnert, S. J. Duffy, A. M. Messmer, R. R. E. Stanley, C. DiBacco & I. R. BradburyUniversity of Aberdeen, Aberdeen, UKK. K. S. LaytonDalhousie University, Halifax, Nova Scotia, CanadaP. Bentzen, S. J. Salisbury & D. E. RuzzanteUniversity of Guelph, Guelph, Ontario, CanadaC. M. Nugent & M. M. FergusonUniversity of Victoria, Victoria, British Columbia, CanadaJ. S. Leong & B. F. Koop More

The polysaccharide xylan limits the growth of C. crescentus cells compared to the monomer xylose in well-mixed environmentsWe first tested our hypothesis that in well-mixed conditions the polymer xylan would limit the productivity of microbial populations relative to the monomer xylose. To determine if this was the case, we grew C. crescentus cells in the same concentration (weight/volume) of either the polymer xylan or its monomeric constituent xylose, both provided as the sole carbon source (Fig. 1a). We then compared the maximum growth rate and the maximal population size over the course of a 54 h growth cycle (Fig. 1b). In line with expectations, populations growing on the monomer xylose achieved higher growth rates and a higher maximum population size (Fig. 1b–d). This was true for all concentrations (0.01–0.1%) of monomer and polymer tested (Supplementary Fig. 2). These findings suggest that in well-mixed environments of equal carbon concentration, the complexity of the growth substrate governs the growth of C. crescentus populations.Cells engage in colonial behaviors on xylan whereas they exhibit solitary behaviors on xyloseGroup formation could be a key mechanism through which cells could overcome polymer-induced growth limitations that exist in well-mixed environments. Collective behavior would allow cells to increase their local cell density, which leads to higher local concentrations of the monomeric products of polymer degradation. To test this prediction, we tested whether xylose and xylan elicit different behavioral responses in C. crescentus. We used microfluidic growth chambers in which cells were forced to grow as a monolayer. Our expectation was that growth within these devices would provide the spatial structure to overcome the growth limitations observed in well-mixed conditions (Supplementary Fig. 1). We tracked and quantified movement, and growth of individual cells using time-lapse microscopy and image analysis. Chambers were constantly replenished with minimal medium containing either xylose or xylan through a main nutrient feeding channel, as described elsewhere [20, 23, 24].We found that C. crescentus displayed strikingly disparate behaviors in xylan and xylose: cells formed microcolonies on the polymer xylan (Fig. 2a, Supplementary Video 1), whereas on the monomer xylose they did not (Fig. 2b, Supplementary Video 2). We analyzed the temporal dynamics of cell growth and movement in the two carbon sources by following individual cells using cell segmentation and tracking. Mapping the lineages based on division events for all the cells in a chamber revealed that the microcolonies on the polymer xylan originated from a single progenitor cell (Fig. 2d, Supplementary Fig. 3a–c; Supplementary Video 3). This finding indicates that microcolonies were a result of swarmer cells not dispersing after division, rather than a product of secondary aggregation by planktonic cells. In contrast, in the monomer xylose only the stalked cells remained in the same position after cell division, whereas the presumably flagellated swarmer cells moved away (Fig. 2e, Supplementary Fig. 4a–c). As a consequence of this difference in behavior, the number of sessile cells increased much more rapidly in xylan. The number of cells in a growth chamber doubled on average every 3.6 ± 0.54 h in xylan (mean ± 95% CI, Fig. 2c) but took 15.50 ± 7.55 h to double in xylose (mean ± 95% CI, Fig. 2c). These differences occurred despite a similar propensity to produce offspring per sessile cell in the two substrates (Supplementary Fig. 5), and thus were driven by the reduced rate at which cells dispersed in xylan.Fig. 2: Cells display solitary behavior on xylose and aggregative behavior on xylan.Representative images of C. crescentus CB15 cells (labeled with constitutively expressed mKate2, false colored as magenta) at different time points within the microfluidic growth chambers supplied with either xylan (a) or xylose (b) as the sole source of carbon. c On xylan (yellow), the number of sessile cells in the growth chamber increases with time, whereas on xylose (blue) it remains nearly constant. Squares indicate the number of cells present at a given time point in each chamber (nchambers = 9), with a linear or exponential regression line for each chamber (xylose, linear regression model, R2 = 0.69–0.92, slope = 1.22–3.27, P  More