Decision Letter | Strong inter-population cooperation leads to partner intermixing in microbial communities

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Strong inter-population cooperation leads to partner intermixing in microbial communities

Decision Letter[highwire:doi]: 
Diethard Tautz, Reviewing editor, Max Planck Institute for Evolutionary Biology, Germany

eLife posts the editorial decision letter and author response on a selection of the published articles (subject to the approval of the authors). An edited version of the letter sent to the authors after peer review is shown, indicating the substantive concerns or comments; minor concerns are not usually shown. Reviewers have the opportunity to discuss the decision before the letter is sent (see review process). Similarly, the author response typically shows only responses to the major concerns raised by the reviewers.

Thank you for choosing to send your work entitled “Cooperation leads to partner intermixing in microbial communities” for consideration at eLife. Your article has been evaluated by a Senior Editor and 3 reviewers, one of whom is a member of our Board of Reviewing Editors.

The Reviewing Editor and the other reviewers discussed their comments before we reached this decision, and the Reviewing Editor has assembled the following comments based on the reviewers’ reports.

The study deals with a very interesting mixture of experimental, theoretical, and simulation approaches to arrive at basic rules of spatial patterning between obligatory cooperative partners in single-celled systems. The studies are based on a previously developed system of two yeast strains that can enter cooperative interactions. The present paper deals with the development of a spatial patterning model in conjunction with a series of experiments that use different starting conditions to infer the stability of the observed patterns. The results of these experiments are then compared with the respective simulation results to validate the theoretical approach. This in turn is taken to infer further, more complex interactions in multi-partner systems. An additional experimental validation comes from the use of two bacterial species that interact on biochemically very different principles.

The referees agree that the paper is very interesting, technically sound, and the whole work rests on a very rich database. The main research question addressed is certainly significant, and the authors elegantly investigate it by using a combination of experimental and theoretical approaches. There are no severe methodological problems that need to be addressed. However, there are some concerns about the generality of the findings. The current version reads in places as if general rules were derived; but, strictly speaking, they are only tested for systems with obligate cooperation. Also, the possibility of antagonistic interactions is not addressed at all. Still, it appears that the paper is a very strong starting point for future work into extended directions. Hence, we will by happy to offer publication in eLife, provided the following points are addressed in a revised version.

A) The authors should be very explicit about the limitations of their current study, as well as the strengths. This could be presented in an extended discussion.

B) One of the reviewers suggests additional experiments in this context, but after further discussions, we consider them to be optional:

“The authors investigate a very special case of cooperation, namely an obligate interaction. Both their synthetic yeast system and the Desulfovibrio–Methanococcus interaction represent a case of an obligate interaction: that is, none of the two partners can grow without the respective other. In this light, the finding that cooperative interactions mix more than other ecological interactions seems much less surprising. It may simply be the consequence of the properties that were previously built into the system by the experimenter (i.e., the obligate mutual dependency) rather than a pattern that generally emerges in cooperative interactions (which are not necessarily obligate in nature). Support the interpretation that the partner intermixing observed by the authors is limited to obligatory cooperation.

Another very prominent example of cooperation in a microbial community is the cooperative production of biofilms (e.g., Rainey & Rainey 2003 Nature). Here we would also see spatial patterns in a biofilm, but I doubt that one would find the enhanced population mixing (given that two biofilm-formers were differentially labeled) as shown by the authors.

A way to manipulate the degree of mutual dependency experimentally would be to add lysine and/or adenine to the medium that is used to grow the yeast strains (as has been done to mimic the commensalism). My expectations for such an experiment would be that with more ‘public goods’ added, the less tight the interaction gets and the less pronounced the population mixing will be. Such an outcome would further support the interpretation that the conclusions drawn do not apply to cooperative interactions within microbial communities in general, but be rather limited to obligate cooperative interactions.”

Please respond to this comment either by doing the experiment or by clearly discussing these points in the manuscript.