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  1. Author Response

    Reviewer #1 (Public Review):

    The authors report the discovery of a new bacterium, termed HS-3, that displays a novel form of multicellularity consisting of long filamentous structures tightly packed into a two-dimensional structure with characteristics reminiscent of liquid crystals. Motivated by the occasional immersion of the bacterial structures in water due to flooding in their cave environment, laboratory immersion is found to disrupt these structures, which can transform into clusters of coccobacillus daughter cells released by contact with water.

    As a discovery, this paper will certainly trigger great interest in this bacterium for these unusual properties. In particular biophysicists studying active matter will be fascinated by the liquid crystalline order and topological defects, which are reminiscent of those in motor/microtubule systems studied recently. The observations of filamentous forms reminds me of the work of Mendelson many years ago on a mutant of B. subtilis that fails to separate daughter colonies after division, leading to growing filaments. But those were not in a colonial form seen here.

    The paper is, however, rather descriptive, without much physical quantification of the biophysical properties. More importantly, the presentation does not make contact with much recent (and not-so-recent) work on the problem of understanding evolutionary driving forces toward multicellularity, particularly as seen in green algae and choanoflagellates.

    We introduced a series of works in the Introduction, Discussion, and Figure 1, in terms of arguments of how single cell organisms could self-organize and sustain the cells in a certain order in the evolutionary process towards multicellularity. Together with the consideration about environmental settings in the cave as an ‘Ecological scaffolding’ and the liquid crystal-like self-organization, the finding of HS-3 was properly contextualized as a new example of multicellularity. As seen in Mendelson’s pioneering work, as well as in recent works on the field of applied hydrodynamics in biology, bacteria have potential to self-organize their cells. However, as far as we know, there is no extant species that clearly shows a relation between liquid crystal phenomenon and the origin of multicellularity. We think the features of HS-3 that we report would serve as an attractive model of bacterial multicellularity useful for future studies including physical analysis and theoretical study.

    Reviewer #2 (Public Review):

    I thought this was a very cool example of bacterial multicellularity, with the description of a newly discovered bacterium that forms a sort of simply differentiated colony- a sheet of cells which then develops to contain a large bolus of small, coccoid cells, which then release into the water column upon submergence. I wasn't totally convinced that this release was developmental, as suggested by the authors- evidence that other colonies released cells at the same time could be due to multiple colonies sharing the same biophysical basis of colony formation that is disrupted by immersion in water (diffusion of extracellular polysaccharides, or even the pressure from being underwater). However, it's notoriously difficult to rigorously test evolutionary hypotheses, and I think that the microbiology here is compelling- it's a form of bacterial multicellularity that I have never seen before.

    My largest issue with the paper is that it does a very poor job of contextualizing how the research affects our understanding of the evolution of multicellularity more broadly. This paper suggests that little is known about the ecological factors selecting for simple multicellularity, but there has actually been quite a bit of work on this topic. This list is far from exhaustive, but prior work has examined a range of selective agents that can favor simple multicellularity- these include predation (Boraas 1998, Herron 2020, Bernardes, 2021), protection from antibiotics (Smukulla 2008), cooperative metabolism (Koschwanez, 2011), dispersal (smith 2014), syntrophy (Libby and Ratcliff, 2021), resource competition (Heaton 2020), and motility / division of labor (Solari 2006). Indeed, one of the things about the evolution of multicellularity is that there is no one 'route'- there are many different reasons different lineages evolve to be multicellular

    The paper is focused around the idea that 'group life' is a hypothetical "missing link" to multicellularity (see Figure 1), but this is not an open hypothesis in the field. It's been a universally accepted fact for more than 50 years. Multicellular organisms had to have evolved from simpler social groups of cells- given their phylogenetic nesting in clades of unicellular organisms, there's no other way they could have come into existence. But there is also been a great deal of work examining simple multicellular relatives of complex multicellular lineages, most notably in the volvocine green algae, holozoans (e.g., choanoflagellates and ichthosporeans), fungi, charophyte algae leading to land plants, and red algae. There is also a body of work using experimental evolution of evolve progressively more complex multicellular lineages (e.g., snowflake yeast). My central problem with this paper is that the 'group phase' they have described is far less compelling than existing work showing a 'group phase' being ancestral to more complex lineages of multicellular organisms, particularly because this multicellular lineage is not contextualized within a clade that has ultimately evolved complex multicellularity.

    In the "recommendations for authors" section, I make suggestions for how to reframe the work to better highlight its novelty, focusing it around a) the discovery of a new form of bacterial multicellularity, and b) the possibility that this reflects ecological scaffolding, a hypothesis for how multicellular organisms could have evolved by developmentally co-opting ecologically-mediated life cycles.

    The manuscript submitted to eLife was actually a different version from the preprint version in bioRxiv, but we noted the comments were based on the preprint version. We apologize for this confusion, if we have missed some submission procedure. The term ‘group life’ has been amended in the present manuscript, and instead we used the term ‘ecological scaffolding’ at the center of the Figure 1, and we think this could correct the wrong impression that evolutionary process is ‘one-route’. We also revised the Introduction to appropriately contextualize HS-3 as a new example of multicellularity among the preceding works, together with references about physiological significance. In the Discussion, we also mentioned some experimental work on evolution including ‘snowflake yeast’ (reference 48 and 49).

    As for the comment about the release of coccoid cells, we also agree that release in water itself is not a programmed developmental process. The “crowded-out” phenomenon was seen on solid agar surface (not in water, Figure 4C), but if we consider the natural niche of HS-3, the significance of the formed structure is the capability to release coccoid cells upon the trigger of immersion in water.

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  2. Evaluation Summary:

    This is a fascinating article on the discovery of an unusual form of bacterial multicellularity: an organism that can exist in dense, filamentous multicellular structures and clusters of coccobacillus daughter cells. Experiments that mimic the periodic immersion that the bacteria experience in their natural cave environment suggest that water immersion plays a role in this life-cycle dynamics. This work, while rather qualitative, will nevertheless likely attract great interest from a diverse range of scientists working on multicellularity, the biophysics of cell packing, and geobiological problems.

    (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. The reviewers remained anonymous to the authors.)

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  3. Reviewer #1 (Public Review):

    The authors report the discovery of a new bacterium, termed HS-3, that displays a novel form of multicellularity consisting of long filamentous structures tightly packed into a two-dimensional structure with characteristics reminiscent of liquid crystals. Motivated by the occasional immersion of the bacterial structures in water due to flooding in their cave environment, laboratory immersion is found to disrupt these structures, which can transform into clusters of coccobacillus daughter cells released by contact with water.

    As a discovery, this paper will certainly trigger great interest in this bacterium for these unusual properties. In particular biophysicists studying active matter will be fascinated by the liquid crystalline order and topological defects, which are reminiscent of those in motor/microtubule systems studied recently. The observations of filamentous forms reminds me of the work of Mendelson many years ago on a mutant of B. subtilis that fails to separate daughter colonies after division, leading to growing filaments. But those were not in a colonial form seen here.

    The paper is, however, rather descriptive, without much physical quantification of the biophysical properties. More importantly, the presentation does not make contact with much recent (and not-so-recent) work on the problem of understanding evolutionary driving forces toward multicellularity, particularly as seen in green algae and choanoflagellates.

    Was this evaluation helpful?
  4. Reviewer #2 (Public Review):

    I thought this was a very cool example of bacterial multicellularity, with the description of a newly discovered bacterium that forms a sort of simply differentiated colony- a sheet of cells which then develops to contain a large bolus of small, coccoid cells, which then release into the water column upon submergence. I wasn't totally convinced that this release was developmental, as suggested by the authors- evidence that other colonies released cells at the same time could be due to multiple colonies sharing the same biophysical basis of colony formation that is disrupted by immersion in water (diffusion of extracellular polysaccharides, or even the pressure from being underwater). However, it's notoriously difficult to rigorously test evolutionary hypotheses, and I think that the microbiology here is compelling- it's a form of bacterial multicellularity that I have never seen before.

    My largest issue with the paper is that it does a very poor job of contextualizing how the research affects our understanding of the evolution of multicellularity more broadly. This paper suggests that little is known about the ecological factors selecting for simple multicellularity, but there has actually been quite a bit of work on this topic. This list is far from exhaustive, but prior work has examined a range of selective agents that can favor simple multicellularity- these include predation (Boraas 1998, Herron 2020, Bernardes, 2021), protection from antibiotics (Smukulla 2008), cooperative metabolism (Koschwanez, 2011), dispersal (smith 2014), syntrophy (Libby and Ratcliff, 2021), resource competition (Heaton 2020), and motility / division of labor (Solari 2006). Indeed, one of the things about the evolution of multicellularity is that there is no one 'route'- there are many different reasons different lineages evolve to be multicellular

    The paper is focused around the idea that 'group life' is a hypothetical "missing link" to multicellularity (see Figure 1), but this is not an open hypothesis in the field. It's been a universally accepted fact for more than 50 years. Multicellular organisms had to have evolved from simpler social groups of cells- given their phylogenetic nesting in clades of unicellular organisms, there's no other way they could have come into existence. But there is also been a great deal of work examining simple multicellular relatives of complex multicellular lineages, most notably in the volvocine green algae, holozoans (e.g., choanoflagellates and ichthosporeans), fungi, charophyte algae leading to land plants, and red algae. There is also a body of work using experimental evolution of evolve progressively more complex multicellular lineages (e.g., snowflake yeast). My central problem with this paper is that the 'group phase' they have described is far less compelling than existing work showing a 'group phase' being ancestral to more complex lineages of multicellular organisms, particularly because this multicellular lineage is not contextualized within a clade that has ultimately evolved complex multicellularity.

    In the "recommendations for authors" section, I make suggestions for how to reframe the work to better highlight its novelty, focusing it around a) the discovery of a new form of bacterial multicellularity, and b) the possibility that this reflects ecological scaffolding, a hypothesis for how multicellular organisms could have evolved by developmentally co-opting ecologically-mediated life cycles.

    Was this evaluation helpful?