Polysaccharide breakdown products drive degradation-dispersal cycles of foraging bacteria through changes in metabolism and motility

  1. Institute of Biogeochemistry and Pollutant Dynamics, Department of Environmental Systems Science, ETH Zurich, Zurich, Switzerland
  2. Department of Environmental Microbiology, Eawag: Swiss Federal Institute of Aquatic Science and Technology, Duebendorf, Switzerland
  3. Geological Institute, Department of Earth Sciences, ETH Zurich, Zurich, Switzerland
  4. Institute of Environmental Engineering, Department of Civil, Environmental and Geomatic Engineering, ETH Zurich, Zurich, Switzerland
  5. Department of Civil and Environmental Engineering, MIT, Cambridge, MA, USA
  6. Department of Biology, University of Southern California, Los Angeles, USA
  7. Institute of Molecular Systems Biology, Department of Biology, ETH Zurich, Zurich, Switzerland
  8. Laboratory of Microbial Systems Ecology, School of Architecture, Civil and Environmental Engineering (ENAC), École Polytechnique Fédéral de Lausanne (EPFL), Lausanne, Switzerland


  • Reviewing Editor
    Babak Momeni
    Boston College, Chestnut Hill, United States of America
  • Senior Editor
    Detlef Weigel
    Max Planck Institute for Biology Tübingen, Tübingen, Germany

Reviewer #1 (Public Review):

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.

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.

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):

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.

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.

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):

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.

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.

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.

  1. Howard Hughes Medical Institute
  2. Wellcome Trust
  3. Max-Planck-Gesellschaft
  4. Knut and Alice Wallenberg Foundation