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  1. Author Response

    Reviewer #1 (Public Review):

    The authors use available structural biology data to compute the energetic cost to build and maintain the activity of flagella in a broad range of unicellular swimming organisms, including bacteria, archaea and eukaryotes. From this energy balance, they try to decipher what advantages the different types of flagellum can provide in terms of motility, feeding and growth. This eventually brings new insights into why bacteria, archaea and eukaryotes have evolved with different types of flagella.

    Strengths:

    The main strength of this study relies on the collection of the data set from three types of unicellular swimming organisms - bacteria, archaea and eukaryotes - for about 200 species. Interestingly, selected species span a large phase space in terms of numbers of flagella/cilia, flagellum length, cell volume... This allows robust analysis and interpretation of the data.

    The method for establishing the energy balance of the construction of complex protein structures seems to be robust. For example, the result obtained by this method to compute the energy cost of E. Coli flagellum is of the same order of magnitude as previously reported values estimated by other methods. This method could be used for other cellular functions for which it is otherwise difficult to estimate the energy cost either experimentally or theoretically.

    Weaknesses:

    The conclusion on the lack of an evolutionary advantage for small cells to swim to find food rather than waiting for food to diffuse is not particularly new. Indeed, Purcell in his famous 1977 paper "life at low Reynolds number" reached the same conclusion by using simple scaling arguments to estimate the trade-off between swimming to find more food and the swimming energy cost.

    We are aware of the result by Purcell, but his estimate of swimming cost only included operating costs of the flagellum, not construction costs. Purcell also didn’t calculate the relative cost of swimming or compare this cost to gains in fitness. We include estimates of both the operating and the construction cost (relative to the whole cell budget), which constitutes a fitness penalty, and compared this to a fitness gain, i.e. an increased growth rate, from swimming in a homogenous environment (Fig. 2F). We made this comparison for many different species (using empirically derived swimming speeds and flagellar costs) and were able to obtain a volume at which swimming in a homogenous environment does yield a net fitness benefit (increased growth rate). Purcell only looked at E coli.

    In the “Flagellar costs and benefits” section, we explicitly contrast our method with what had been done before (citing Wan et al., Phil. Trans. R. Soc. B 2021) and indicate the improvements that we made (i.e. adding construction cost and calculating a net fitness effect).

    We have now added the Purcell 1977 paper as a reference.

    Although the method does have strengths in principle, the weakness of the paper is that the main conclusions are not discussed enough or put in perspective with regards to the initial aims of the paper: better understand why three different types of flagellum exist. In particular, the fact that "there is no detectable difference in the cost-effectiveness of generating swimming speed between eukaryotic and prokaryotic flagella" is not really discussed. One of the major characteristics of eukaryotes is that they have evolved into more complex multicellular forms of life where multiciliated cells are ubiquitous and support more diverse physiological functions (transport, washing surface...) than swimming. So maybe an evolutionary advantage of eukaryotic flagella over prokaryotic flagella should be discussed in that context.

    We do apply our findings to the problem of the different types of flagella in the section “Evolution of the eukaryotic flagellum”, where, among other things, we discuss the possible consequences of the bacterial and eukaryotic cell sizes and the disparate flagellar mechanisms (especially the different flagellar sizes) for the distribution of flagellar types across the tree of life. We did indeed not discuss differences in abilities between eukaryotic and bacterial flagella aside from the ability to generate speed. The eukaryotic flagellum may, by virtue of its distribution of motor proteins throughout its length, be able to generate beats that the bacterial flagellum is not capable of, potentially giving the eukaryote enhanced agility (ability to turn). We did not include these considerations because we are unaware of systematic data on agility that would allow us to compare the capacities of bacterial and eukaryotic flagella. Also, the investment in a single eukaryotic flagellum could pay for multiple prokaryotic flagella, which together may provide the same level of agility as a single eukaryotic flagellum.

    We feel that the functions of eukaryotic flagella in multicellular species, although interesting in and of themselves, don’t bear on the issue of the evolution of the eukaryotic flagellum, as this flagellum was long established before the multicellular species arose. It is also not clear whether the eukaryotic flagellum would do a better job than the prokaryotic flagellum in various multicellular tasks.

    We have added some of these considerations to the discussion.

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  2. Evaluation Summary:

    This work will be of interest to readers in the fields of cell biology, evolutionary biology, and biophysics. The collected data are of good quality and are properly analysed. The work thus convincingly demonstrates that energetic considerations (building costs versus potential benefit) must be taken into account to understand flagellar evolution.

    (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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  3. Reviewer #2 (Public Review):

    In their work Schavemaker & Lynch aim to understand the reason for the structural differences between the bacterial, archaeal and eukaryotic flagella. Using structural data of three model organisms, which represent three domains of life, the authors have determined the energy costs of building and operating flagella. They further expand their analysis to additional 196 species, using morphological data from the literature about their flagella and cell volume. To evaluate cost-effectiveness of the flagella, the authors analyzed their effect on swimming speed, nutrient uptake, and cell growth. The reason for the structural differences between the different types of flagella remained an enigma for decades. In their work, the authors offer a fascinating and convincing approach to explain the reason for these differences. Energetic considerations appear to be critical for the evolution and maintenance of flagella. Interestingly, the data also indicate flagellar proteins experience different evolutionary forces due to differences in the energetic costs caused by the protein copy-number. The conclusions of this paper are mostly well supported by data. Yet, a few key structural elements are missing in the calculated construction cost of the eukaryotic flagella. This may affect the authors' estimations and conclusions.

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  4. Reviewer #1 (Public Review):

    The authors use available structural biology data to compute the energetic cost to build and maintain the activity of flagella in a broad range of unicellular swimming organisms, including bacteria, archaea and eukaryotes. From this energy balance, they try to decipher what advantages the different types of flagellum can provide in terms of motility, feeding and growth. This eventually brings new insights into why bacteria, archaea and eukaryotes have evolved with different types of flagella.

    Strengths:

    The main strength of this study relies on the collection of the data set from three types of unicellular swimming organisms - bacteria, archaea and eukaryotes - for about 200 species. Interestingly, selected species span a large phase space in terms of numbers of flagella/cilia, flagellum length, cell volume... This allows robust analysis and interpretation of the data.

    The method for establishing the energy balance of the construction of complex protein structures seems to be robust. For example, the result obtained by this method to compute the energy cost of E. Coli flagellum is of the same order of magnitude as previously reported values estimated by other methods. This method could be used for other cellular functions for which it is otherwise difficult to estimate the energy cost either experimentally or theoretically.

    Weaknesses:

    The conclusion on the lack of an evolutionary advantage for small cells to swim to find food rather than waiting for food to diffuse is not particularly new. Indeed, Purcell in his famous 1977 paper "life at low Reynolds number" reached the same conclusion by using simple scaling arguments to estimate the trade-off between swimming to find more food and the swimming energy cost.

    Although the method does have strengths in principle, the weakness of the paper is that the main conclusions are not discussed enough or put in perspective with regards to the initial aims of the paper: better understand why three different types of flagellum exist. In particular, the fact that "there is no detectable difference in the cost-effectiveness of generating swimming speed between eukaryotic and prokaryotic flagella" is not really discussed. One of the major characteristics of eukaryotes is that they have evolved into more complex multicellular forms of life where multiciliated cells are ubiquitous and support more diverse physiological functions (transport, washing surface...) than swimming. So maybe an evolutionary advantage of eukaryotic flagella over prokaryotic flagella should be discussed in that context.

    Overall the data presented in this study support the conclusions of the paper, which are not overclaimed.

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