Exploring how the fast-slow pace of life continuum and reproductive strategies structure microorganism life history variation

  1. Josje Romeijn
  2. Isabel Smallegange

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Abstract

Studying life history strategies in microorganisms can help predict their performance when complex microbial communities can be categorised into groups of organisms with similar strategies. Microorganisms are typically classified as copiotroph or oligotroph, but it has been proven difficult to generalise their life history strategies to broad lineages. Here we tested if the fast-slow continuum and reproductive strategy framework of macro-organismal life histories can be applied to microorganisms. We used demographic and energy budget data from 13 microorganisms (bacteria, fungi, a protist and a plant) to examine how generation time, survivorship, growth form, age at maturity, recruitment success, and net reproductive rate structure microbial life histories. We found that 79% of microorganism life-history variation fell along two uncorrelated axes. Like macro-organisms, we found a fast–slow pace of life continuum, including shorter-lived microorganisms at one end, and longer-lived microorganisms that mature later in life at the other. Also, like macro-organisms, we found a second, reproductive strategy axis, with microorganisms with greater lifetime reproductive success and decreased mortality at older age at one end, and microorganisms with the opposite characteristics at the other end. Microorganismal life history strategies did not covary proportionally to their shared evolutionary history. Thus, whereas this work suggests that the macro-organismal fast-slow continuum and reproductive strategy framework could be realistically applied to microorganisms, their life history processes cannot be inferred from patterns in taxonomic composition.

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  1. Access Microbiology

    The rationale behind this work is interesting, but the reviewers raise several concerns that must be addressed. Specifically, there are legitimate concerns around the phylogenetic analysis, the chosen dataset, and the terminology used throughout to describe microorganisms. A significant proportion of the text is also identical to published work by Smallegange and Lucas (unreferenced).

  2. Access Microbiology

    Comments to Author

    Overview: This manuscript uses a dynamic energy budget (DEB) modeling approach to explore ideas related to the life history of 13 microorganisms. The model relies on information on cell size (at birth, at division, and maximum) from the literature. The DEB is then used to estimate life history traits, including generation time, shape of the survivorship curve, age at maturity, progressive growth, retrogressive growth, recruitment success, and net reproductive rate. The paper then describes variation in these estimated life history traits using PCA along with some tests to determine whether the traits evolve randomly with respect phylogeny (i.e., Brownian motion). The paper seems to be particularly focused on identifying patterns that would be consistent with a fast-slow reproductive strategy that is commonly associated with copiotroph vs. oligotroph classifications in the microbial literature. Major concerns: I'm not an expert in DEBs, but my sense is that such approaches have not been widely applied to microorganisms. Therefore, I was really excited to see what we might learn in this paper about life history using a framework that was developed for understanding plant and animal life history. Despite my initial optimism, ultimately, I was left with a bit of confusion and concern: - I have some reservations about the data set. First, a lot of inferences are being made from 13 taxa. I'm afraid that this does not constitute enough observation for making strong and/or broad inference. Perhaps I would be less critical about this if the data required for each taxon was harder to come by. But Table 1 reveals that the inputs effectively boil down to cell size measurements that are in turn used to estimate growth (von Bertalanffy). I can believe that maybe such data are not widely available in the literature, perhaps because length at birth (Lb), length at division (Ld), and maximum length (Lm) are not commonly measured. That being said, I think it would not be difficult to generate such data for a larger collection of taxa. - In addition to the small number of taxa, the choice of taxa is a bit strange. I don't think it's appropriate to call Chlamydomonas a "plant"; it's a phototrophic protist (i.e., algae). Across the 13 taxa, the metabolisms are quite varied, and I'm not sure this works as an advantage to the study. Some representatives are phototrohs (Synechococcus, Chlamydomonas), some are predatory (Dictyostelium), some are chemoorganoheterotrophs (e.g., yeast, E. coli, B. subtilis), and others are sulfate reducers (Desulfovibrio) or methylotrophs (Methulorubrum). Combined with the small number of taxa, I'm not sure that this helps with making generalization about broad lineages, which is one of the stated goals of the paper (line 295). - I'm concerned about the phylogenetic analyses, specifically the construction of the tree. Most of the description seems to be contained in the caption for Fig. 1. Thus, I'm unclear as to what gene(s) were used for sequence alignment. This is important because the strains span multiple domains of life (Bacteria and Eukaryotes), which diverged billions of years ago. Thus, I would expect branch lengths to look very different from what is presented in Fig. 1. Is this a supertree? That is, a larger tree constructed from smaller trees? The answers to these questions will help with evaluating inferences about the role of phylogeny in life history patterns. Without a clearer description of these data and methods, I cannot trust the conclusions from the phylogenetic PCA or Pagel's lambda. - There is some strange wording in the paper where macroorganism-related concepts don't translate so seamlessly into the microbial field, which is important given where manuscript was submitted. For example, with the exception of Dictyostelium, none of the taxa "ingest" resources in the traditional sense (see text starting on line 90), which means that assimilation efficiency (epsilon) is a little odd. Rather, they are osmotrophs that "uptake" or "consume" resources across their membranes, such that assimilation efficiency is not typically considered (e.g., there is no "sloppy feeding"). - I was also confused by "somatic growth" which often implies cellular differentiation. In multiple places (e.g., Table 2 caption), the paper refers to sexual reproduction or "sexual maturity"; while this can occasionally happen with some of the eukaryotic microbes, my sense is that this must not be related to the current project. Rather, it seems to be due to the fact that the text has been reproduced verbatim from another paper (Smallegange and Lucas 2024, Scientific Data: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10834990/). - I'm puzzled by some of the wording and/or assumptions about reproduction and mortality. There are actually some pretty important distinctions when it comes to division and mortality for the taxa under investigation. For example, Caulobacter is unique in that the mother cell typically forms a stalk to an attached surface and produces rejuvenated offspring via budding, while aging. Yeasts produce offspring via budding and thus experience replicative aging. Meanwhile, other microbes in the list undergo binary fission. But what I found strange were statements like "division is fatal" (line 175), "all individuals die after reproducing" (line 230), "reproduction in microorganisms entails that the dividing individual ceases to exist". Taken at face value this seems weird, but I can see, for example, on line 199 that no = 2, which means that "one microorganism divides to produce two offspring. So perhaps this last issue is semantic or can be resolved in a mathematical sense, but it is also a little confusing in light of microbial reproduction. - I think more could be done to explain, justify, and translate parameters in Table 2 and how this information is later used to support the conclusion of there being trade-offs in "reproductive strategy". - Based on the above observations, I came away with the sense that this study was perhaps motivated by the opportunity to apply a quantitative method to a group of organisms for which more careful consideration about biology was needed. - I had some questions about the raw data that was used to run the DEBs (Table 1). For a number or columns (k, u, no) the values across taxa are invariant. Meanwhile, the size measurements, which are the primary inputs, are all highly correlated. So, how much of the major findings are just due to allometry or body size relationships and how we know this affects organismal biology? - Somewhat related, there seems to be an outlier that the authors may want to look into: why does E. coli have a growth rate that is so much higher than other microbes. For example, E. coli and Pseudomonas aeruginosa have generation time (reported in the literature) that are quite comparable; certainly not 20-fold different as suggested by data in Table 1. If this is not a typo, then it would be useful to know how Bertalanffy growth rate is so high for this species compared to all others. When I plotted cell size vs. rB, this observation is an obvious outlier in all instances. - I'm skeptical of the copiotroph/oligotroph classification system in Figure 1. By what criterion are Chlamydomonas or Synechococcus assigned "oligotroph", or Mycobacterium a copiotroph? (Also "Mycolicibacterium" is spelled wrong in Fig. 1). This becomes important and somewhat circular when it comes to "confirming" results (Fig. 2).

    Please rate the manuscript for methodological rigour

    Poor

    Please rate the quality of the presentation and structure of the manuscript

    Poor

    To what extent are the conclusions supported by the data?

    Not at all

    Do you have any concerns of possible image manipulation, plagiarism or any other unethical practices?

    Yes: some of the text seems to come directly from another published paper by the authors, including nearly exact reproduction of Table 2: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10834990/

    Is there a potential financial or other conflict of interest between yourself and the author(s)?

    No

    If this manuscript involves human and/or animal work, have the subjects been treated in an ethical manner and the authors complied with the appropriate guidelines?

    Yes

  3. Access Microbiology

    Comments to Author

    General comments: This paper is an examination of microbial life history patterns through the adaptation of a two-axis macro-organismal framework (1. Fast-slow growth and lifespan, 2. Reproductive strategy). The authors test the applicability of this framework on 13 microbial species spanning bacterial and eukaryote lineages. They identified support for this framework along the axis of fast vs. slow pace of life but not along the reproductive axis. The authors conclude that both axes can be used as a predictive framework to supplement existing ideas. In general I do not find the methods or results compelling and I do not see this paper, as currently constructed, as being a useful addition to the ongoing discussion of microbial life history strategies. While the concept is intriguing, it must be explored and described with more rigor (i.e. substantial revisions). Some thoughts: - I do not believe that 13 species can adequately be used to support the conclusions from the authors, even for an exploratory work. I would suggest a greater number of species be included in the analysis, including Archaea. Along those lines, the authors need to include their methods for choosing specific lineages, identifying phylogenetic relationships, and making taxonomic assignments. I am concerned with the use of the OTL for identifying and categorizing microorganisms which as I understand, it is not well-suited to do. At least, it is not used by microbiologists and microbial ecologists. The field has moved towards trait exploration at a large scale either through bacterial trait databases from cultured isolates (BactoTrait and BacDive) or from the increasing data available from metagenomic, metatranscriptomic, and metaproteomic studies (microTrait). I can appreciate the authors efforts as analogous to those of Cebron et al. in 2021 (https://doi.org/10.1016/j.ecolind.2021.108047) but they must scale-up. - Related to the issue of bringing more organisms into the analysis, the paper does not outline the methodology and reasoning for the selection of organisms it does include. At the very least, one paragraph of methods should be dedicated towards the intent and origin of microbial organisms (i.e., where and why), alignment into a single phylogeny, and assignment into life history clusters. - Related to life history assignments: the life-history assignments of many of the bacterial species from Stone et al. do not always match with Genera identified in their supplemental reporting, and sometimes do not follow the life history strategies reported. The authors need to correct any inconsistencies and update their methods if they re-assigned the provided 16S sequences to new taxonomies. See detailed comments. - The trends are reported with little statistical support. Why not at least perform a PERMNOVA between clusters? Specific comments: I am concerned with the use of the OTL for microorganisms which as I understand it is not well-suited to do. I am concerned with the small sampling extent of the microorganisms. 13 species are not representative of the life history trait extent of all microorganisms and modern trait explorations typically undertake a greater number of organisms. Where is the description and methodology for obtaining microorganisms, trait assignments, and phylogenetic relationships? Figure 1: I am concerned with the assignment of organisms into taxonomic clusters from the Stone 2023 paper. Several lineages are not identified in Stone's supplemental list of life history strategies. And in some cases a lineages is given an assignment in conflict with Stone. - Species 2. Chlamydomonas reinhardtii. Stone et al. only explored bacterial life history strategies -- please update with the correct citation - Species 4. Synechococcus elongatus - Species 5. Mycolicibacterium smegmatis. Mycobacterium is a listed genus in Stone's supplemental table but it clustered most frequently under oligotrophic life history strategies, not copiotrophic as here - Species 7. Shewanella oneidensis - Species 8. Escherichia coli The panels in figure 2 seem redundant since they closely align. I suggest moving one to supplemental and presenting only one of the figures. L230-231: The authors should be careful about distinguishing the model condition of having a parent cell "die" following binary fission from the biological reality. While it is clear that this parameterization is a modeling necessity of bringing the DEB-IPM to microorganisms, the language should be clear throughout the paper. My suggestion would be to change "Because all individuals die after reproducing" to something like "Because death of the parent cell is a necessity to represent microbial reproduction in DEB-IBM" L263-266: This interpretation is only supported due to the assignment of organisms to distinct trait strategies which I have identified concerns about. Does this statement have statistical support? What about a PERMANOVA? L282-283: As above, does this statement have statistical support? L288-292: Could a lack of phylogenetic signal be due to low number of species? L302-304: This suggestion is not supported by the data, especially not for the second axis which was described as a complete overlap between expected strategies. The authors should clarify how their findings demonstrate a limitation in the current scheme or extend the current paradigm.

    Please rate the manuscript for methodological rigour

    Poor

    Please rate the quality of the presentation and structure of the manuscript

    Good

    To what extent are the conclusions supported by the data?

    Partially support

    Do you have any concerns of possible image manipulation, plagiarism or any other unethical practices?

    No

    Is there a potential financial or other conflict of interest between yourself and the author(s)?

    No

    If this manuscript involves human and/or animal work, have the subjects been treated in an ethical manner and the authors complied with the appropriate guidelines?

    Yes

  4. Version published to 10.1099/acmi.0.000769.v1 on Access Microbiology