Polysaccharide breakdown products drive degradation-dispersal cycles of foraging bacteria through changes in metabolism and motility
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eLife assessment
This manuscript is a valuable contribution to our understanding of foraging behaviors in marine bacteria. The authors present a conceptual model for how a marine bacterial species consumes an abundant polysaccharide. Using experiments in microfluidic devices and through measurements of motility and gene expression, the authors offer solid evidence that the degradation products of polysaccharide digestion can stimulate motility.
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Abstract
Most of Earth’s biomass is composed of polysaccharides. During biomass decomposition, polysaccharides are degraded by heterotrophic bacteria as a nutrient and energy source and are thereby partly remineralized into CO 2 . As polysaccharides are heterogeneously distributed in nature, following the colonization and degradation of a polysaccharide hotspot the cells need to reach new polysaccharide hotspots. Even though these degradation-dispersal cycles are an integral part in the global carbon cycle, we know little about how cells alternate between degradation and motility, and which environmental factors trigger this behavioral switch. Here, we studied the growth of the marine bacterium Vibrio cyclitrophicus ZF270 on the abundant marine polysaccharide alginate. We used microfluidics-coupled time-lapse microscopy to analyze motility and growth of individual cells, and RNA sequencing to study associated changes in gene expression. Single cells grow at reduced rate on alginate until they form large groups that cooperatively break down the polymer. Exposing cell groups to digested alginate accelerates cell growth and changes the expression of genes involved in alginate degradation and catabolism, central metabolism, ribosomal biosynthesis, and transport. However, exposure to digested alginate also triggers cells to become motile and disperse from cell groups, proportionally increasing with the group size before the nutrient switch, accompanied by high expression of genes involved in flagellar assembly, chemotaxis, and quorum sensing. The motile cells chemotax toward alginate hotspots, likely enabling cells to find new polysaccharide hotspots. Overall, our findings reveal the cellular mechanisms underlying bacterial degradation-dispersal cycles that drive remineralization in natural environments. Polysaccharides, also known as glycans, are the most abundant form of biomass on Earth and understanding how they are degraded by microorganisms is essential for our understanding of the global carbon cycle and the storage and release of CO 2 by natural systems. Although group formation is a common strategy used by bacterial cells to degrade ubiquitous polymeric growth substrates in nature, where nutrient hotspots are heterogeneously distributed, little is known about how cells prepare for dispersal from an exhausted nutrient source and re-initiate degradation of new nutrient patches. By quantifying growth, motility and chemotaxis of individual cells and comparing gene expression changes when populations were exposed to either polysaccharides or their degradation products in the form of digested polysaccharides, we show that bacterial cells alter their behavior when they experience a shift from polymeric to digested polysaccharides: After cells form groups during growth on polymers, the exposure to degradation products made cells motile, enabling dispersal from sessile cell groups and - guided by chemotaxis - movement towards new polysaccharide hotspots. Our study sheds light on the cellular processes that drive bacterial growth and behavior during carbon remineralization, an important driver of CO 2 release from biomass in natural systems.
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eLife assessment
This manuscript is a valuable contribution to our understanding of foraging behaviors in marine bacteria. The authors present a conceptual model for how a marine bacterial species consumes an abundant polysaccharide. Using experiments in microfluidic devices and through measurements of motility and gene expression, the authors offer solid evidence that the degradation products of polysaccharide digestion can stimulate motility.
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Reviewer #1 (Public Review):
Summary:
The authors attempt to understand how cells forage for spatially heterogeneous complex polysaccharides. They aimed to quantify the foraging behavior and interrogate its genetic basis. The results show that cells aggregate near complex polysaccharides, and disperse when simpler byproducts are added. Dispersing cells tend to move towards the polysaccharide. The authors also use transcriptomics to attempt to understand which genes support each of these behaviors - with motility and transporter-related genes being highly expressed during dispersal, as expected.Strengths:
The paper is well written and builds on previous studies by some of the authors showing similar behavior by a different species of bacteria (Caulobacter) on another polysaccharide (xylan). The conceptual model presented at the end …Reviewer #1 (Public Review):
Summary:
The authors attempt to understand how cells forage for spatially heterogeneous complex polysaccharides. They aimed to quantify the foraging behavior and interrogate its genetic basis. The results show that cells aggregate near complex polysaccharides, and disperse when simpler byproducts are added. Dispersing cells tend to move towards the polysaccharide. The authors also use transcriptomics to attempt to understand which genes support each of these behaviors - with motility and transporter-related genes being highly expressed during dispersal, as expected.Strengths:
The paper is well written and builds on previous studies by some of the authors showing similar behavior by a different species of bacteria (Caulobacter) on another polysaccharide (xylan). The conceptual model presented at the end encapsulates the findings and provides an interesting hypothesis. I also find the observation of chemotaxis towards the polysaccharide in the experimental conditions interesting.Weaknesses:
Much of the genetic analysis, as it stands, is quite speculative and descriptive. I found myself confused about many of the genes (e.g., quorum sensing) that pop up enriched during dispersal quite in contrast to my expectations. While the authors do mention some of this in the text as worth following up on, I think the analysis as it stands adds little insight into the behaviors studied. However, I acknowledge that it might have the potential to generate hypotheses and thus aid future studies. Further, I found the connections to the carbon cycle and marine environments in the abstract weak --- the microfluidics setup by the authors is nice, but it provides limited insight into naturalistic environments where the spatial distribution and dimensionality of resources are expected to be qualitatively different. -
Reviewer #2 (Public Review):
Summary:
The paper sets out to understand the mechanisms underlying the colonization and degradation of marine particles using a natural Vibrio isolate as a model. The data are measurements of motility and gene expression using microfluidic devices and RNA sequencing. The results reveal that degradation products of alginate do stimulate motility but not chemotaxis. The evidence for these claims is strong. The story of how particle degradation occurs through colonization and dispersal has modest support in the data. A quantitative description of these dynamics awaits future studies.Strengths:
The microfluidic and transcriptional measurements are the central strengths of the paper as they allow the delineation of phenotypes at the cellular and molecular levels in the presence of polymer and byproducts of …Reviewer #2 (Public Review):
Summary:
The paper sets out to understand the mechanisms underlying the colonization and degradation of marine particles using a natural Vibrio isolate as a model. The data are measurements of motility and gene expression using microfluidic devices and RNA sequencing. The results reveal that degradation products of alginate do stimulate motility but not chemotaxis. The evidence for these claims is strong. The story of how particle degradation occurs through colonization and dispersal has modest support in the data. A quantitative description of these dynamics awaits future studies.Strengths:
The microfluidic and transcriptional measurements are the central strengths of the paper as they allow the delineation of phenotypes at the cellular and molecular levels in the presence of polymer and byproducts of polymer degradation.Weaknesses:
The explanation of the microfluidics measurements is somewhat confusing but I think this could be easily remedied. The quantitative interpretation of the dispersal data could also be improved and I'm not clear if the data support the claim made. -
Reviewer #3 (Public Review):
Summary:
In this manuscript, Stubbusch and coauthors examine the foraging behavior of a marine species consuming an abundant marine polysaccharide. Laboratory experiments in a microfluidic setup are complemented with transcriptomic analyses aiming at assessing the genetic bases of the observed behavior. Bacterial cells consuming the polysaccharide form cohesive aggregates, while they start dispersing away when the byproduct of the digestion of the polysaccharide starts accumulating. Dispersing cells, tend to be attracted by the polysaccharide. Expression data show that motility genes are enriched during the dispersal phase, as expected. Counterintuitively, in the same phase, genes for transporters and digestions of polysaccharides are also highly expressed.Strengths:
The manuscript is very well written and …Reviewer #3 (Public Review):
Summary:
In this manuscript, Stubbusch and coauthors examine the foraging behavior of a marine species consuming an abundant marine polysaccharide. Laboratory experiments in a microfluidic setup are complemented with transcriptomic analyses aiming at assessing the genetic bases of the observed behavior. Bacterial cells consuming the polysaccharide form cohesive aggregates, while they start dispersing away when the byproduct of the digestion of the polysaccharide starts accumulating. Dispersing cells, tend to be attracted by the polysaccharide. Expression data show that motility genes are enriched during the dispersal phase, as expected. Counterintuitively, in the same phase, genes for transporters and digestions of polysaccharides are also highly expressed.Strengths:
The manuscript is very well written and easy to follow. The topic is interesting and timely. The genetic analyses provide a new, albeit complex, angle to the study of foraging behaviors in bacteria, adding to previous studies conducted on other species.Weaknesses:
I find this paper very descriptive and speculative. The results of the genetic analyses are quite counterintuitive; therefore, I understand the difficulty of connecting them to the observations coming from experiments in the microfluidic device. However, they could be better placed in the literature of foraging - dispersal cycles, beyond bacteria. In addition, the interpretation of the results is sometimes confusing. -
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