Particle foraging strategies promote microbial diversity in marine environments
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Evaluation Summary:
This manuscript explores how microbial foraging strategies contribute to species coexistence in aquatic environments, and will be of interest to microbial ecologists and theoretical ecologists. Using mathematical modeling, the authors demonstrate that differences in particle detachment rates across bacterial species can promote coexistence. Additional explanation and documentation of methods, along with a discussion of the generality of the results, would strengthen the manuscript and ensure reproducibility.
(This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. Reviewer #1 agreed to share their name with the authors.)
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Abstract
Microbial foraging in patchy environments, where resources are fragmented into particles or pockets embedded in a large matrix, plays a key role in natural environments. In the oceans and freshwater systems, particleassociated bacteria can interact with particle surfaces in different ways: some colonize only during short transients, while others form longlived, stable colonies. We do not yet understand the ecological mechanisms by which both shortterm and longterm colonizers can coexist. Here, we address this problem with a mathematical model that explains how marine populations with different detachment rates from particles can stably coexist. In our model, populations grow only while on particles, but also face the increased risk of mortality by predation and sinking. Key to coexistence is the idea that detachment from particles modulates both net growth and mortality, but in opposite directions, creating a tradeoff between them. While slowdetaching populations show the highest growth return (i.e., produce more net offspring), they are more susceptible to suffer higher rates of mortality than fastdetaching populations. Surprisingly, fluctuating environments, manifesting as blooms of particles (favoring growth) and predators (favoring mortality) significantly expand the likelihood that populations with different detachment rates can coexist. Our study shows how the spatial ecology of microbes in the ocean can lead to a predictable diversification of foraging strategies and the coexistence of multiple taxa on a single growthlimiting resource.
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Evaluation Summary:
This manuscript explores how microbial foraging strategies contribute to species coexistence in aquatic environments, and will be of interest to microbial ecologists and theoretical ecologists. Using mathematical modeling, the authors demonstrate that differences in particle detachment rates across bacterial species can promote coexistence. Additional explanation and documentation of methods, along with a discussion of the generality of the results, would strengthen the manuscript and ensure reproducibility.
(This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. Reviewer #1 agreed to share their name with the authors.)

Reviewer #1 (Public Review):
The premise of this paper is that a significant amount of microbial diversity might be maintained not purely through resource partitioning, as has been the thrust of multiple recent papers over the last few years, but perhaps also through "physical" differences between organismshere manifested by the detachment rate of heterotrophic bacteria from resources in the form of particulate matter. I completely agree with that premise, and agree that this is an underexplored niche axis that is important to account for when seeking to understand coexistence and diversity.
As with any mathematical model, the assumptions made are critical to get right, and different assumptions about the details of resource uptake, dispersal, and competition may lead to different conclusions. So my comments primarily relate to some …
Reviewer #1 (Public Review):
The premise of this paper is that a significant amount of microbial diversity might be maintained not purely through resource partitioning, as has been the thrust of multiple recent papers over the last few years, but perhaps also through "physical" differences between organismshere manifested by the detachment rate of heterotrophic bacteria from resources in the form of particulate matter. I completely agree with that premise, and agree that this is an underexplored niche axis that is important to account for when seeking to understand coexistence and diversity.
As with any mathematical model, the assumptions made are critical to get right, and different assumptions about the details of resource uptake, dispersal, and competition may lead to different conclusions. So my comments primarily relate to some of these mathematical choices, as well as to their explanation in the text.
 In framing the paper, I think the authors are right to focus on dispersal and detachment as underexplored mechanisms. But readers will benefit from reference to other work (even on particleassociated microbes) related to resource diversity, succession, and crossfeeding. That can only help put the current study in context with other mechanisms for the maintenance of microbial diversity.
 There is a population growth process when a cell settles on a new particle. This is assumed to be logistic growth, though in the end, it seems likely that the precise dynamics of the growth process don't matter so much as the final abundance (carrying capacity). However, this seemed subtle to me for three reasons:
(i) Will detachment rate directly affect carrying capacity?
(ii) Is carrying capacity occurring when microbes fill out the surface of a particle, or when they have eaten the entire volume of a particle?
(iii) If the former, will particles continue to be shed from the particle as growth continues approximately linearly?
It's possible that none of this matters too much if all that's important is a final population size. However, it might help to clarify the process for readers if we have a conceptual picture of what this final population size represents (surface of particle being filled? or volume of particle entirely eaten up) and if there is a truer picture of the dynamics than logistic growth.
 The relationship between the tradeoff (between different detachment rates) derived in Eq 2 versus the optimal detachment rate (derived in the methods) is framed a little confusingly. If I understand correctly, the "tradeoff" actually comes from the condition that a population will have net nonnegative growth rate in the absence of other populations with different strategies. So it may be reasonable to frame this as a thresholda necessary condition rather than a sufficient condition for a given population to persist. The reason I say this is that it is a bit confusing to have a tradeoff that suggests a range of detachment rates can coexist so long as they differ in their carrying capacities, since it is then stated that the optimal detachment rate outcompetes all the others. Maybe I misunderstood something important being assumed about the carrying capacity for the optimal case, but a tradeoff that also has an optimum is an odd outcome.
 In the end, it seems critical that for multiple strategies to be maintained in the population that there is not only wholeparticle mortality (which in effect is highly correlated catastrophic dynamics for an individual microbial population), but that the inflow of resources itself fluctuates. Did I interpret that correctly? Readers may appreciate a slightly clearer description of how this environmental stochasticity differs from the previous possibility of wholecell mortality, and this also left me wondering how to quantity the kind of environmental stochasticity that will generally lead to multiple strategies coexisting.
 In summary, I think this is a terrific idea and promising analysis that will bear fruit. But I also wanted to understand how robust is the outcome of coexistence to the various assumptions in the model.

Reviewer #2 (Public Review):
Using a mathematical model of particleassociated bacteria growth, detachment and colonization, the authors found that bacteria with different detachment rates can coexist at steady state only in the presence of particlewide mortality, via a tradeoff between net growth and mortality on particles. This phenomenon is remindful of the competitioncolonization tradeoff, an ecological mechanism used to explain diversity via a tradeoff between colonizing and survival abilities, but is distinct from it as the two species considered here only differ for the rate at which they detach from particles. Species with low detachment rates can reap the growth benefits of residing for longer on particles consuming particulate organic matter, but face an increased mortality due to increased risk of predation and viral …
Reviewer #2 (Public Review):
Using a mathematical model of particleassociated bacteria growth, detachment and colonization, the authors found that bacteria with different detachment rates can coexist at steady state only in the presence of particlewide mortality, via a tradeoff between net growth and mortality on particles. This phenomenon is remindful of the competitioncolonization tradeoff, an ecological mechanism used to explain diversity via a tradeoff between colonizing and survival abilities, but is distinct from it as the two species considered here only differ for the rate at which they detach from particles. Species with low detachment rates can reap the growth benefits of residing for longer on particles consuming particulate organic matter, but face an increased mortality due to increased risk of predation and viral infection. Conversely, species with high detachment rates elude such risks, at the expense of a reduced growth benefit. This manuscript adds to the recently renewed interest on applications of optimal foraging theory to the study of microbial growth on marine snow.
The strengths of this work are that the results have a clear intuitive explanation and that the parameters used for the analysis are realistic, except perhaps for those related to bacteriaparticle encounter rates that are not well explained in the manuscript and ignore bacterial motility, which can greatly increase their effective diffusion coefficient with respect to the StokesEinstein estimate used in this work. The authors have investigated a broad range of parameters to provide generality to their numerical results. The relationship between differences of particle detachment rates and biodiversity is, to the best of my knowledge, original, and interesting.
The simulation data presented in the paper support the claims put forth by the authors, but some imprecisions and gaps in the methods section limit the reproducibility of their results in the current version of the manuscript. For example, the details of bacteriaparticle encounter rates are insufficiently explained in the methods section, given that the expression for the encounter rate alpha is never reported explicitly. Publication of the computer code (not available at this stage) would clarify these doubts and allow assessing the validity of the results with more confidence.
Together with other papers published recently from this and other groups, this manuscript expands our understanding of the factors affecting the foraging strategies and coexistence of microbial species on particles. This manuscript focused exclusively on detachment rates, but many other strategies are thought to affect the growth and diversity of particleassociated microbial communities, such as attachment strategies (Yawata et al, PNAS 15:11, 2015), nutrient concentration sensing (Yawata et al, PNAS 117:41, 2020), microbial interactions (Datta et al, Nature Communications 7:11965, 2016), and others (Fernandez et al, The ISME Journal 13, 2019). Although it makes sense to focus on a single process for the purposes of this investigation, a broader discussion of the relationship between the role of detachment rates and other relevant quantities is warranted in the discussion section to clarify the generality and limitations of this work. For example, differences in relevant traits such as search strategy, motility and metabolic interactions may also affect coexistence on particles.
