Glen, thank you; these are excellent, 

The "GASP phenotype” is indeed exactly the keyword I was responding to and, 
characteristically, couldn’t remember the name of.

Whether any of these speakers was the one I heard at my own first exposure, I 
can’t recall.  But I haven’t read any of the papers below (and only “have" 
Lennon/Shoemaker but have not read it yet either), so they actually need to go 
onto my reading list.  Thank you for all of them.  This is general stuff I 
should know.

Result is that I can’t, yet, pick a best exemplar.  But some form of 
contact-tracing, either forward or backward, from these, will surely lead to it.

Just off a breathless few weeks, and sweeping my head back into at least 
something like a pile, so I will be slow.  But these kinds of topics are where 
I want to be, so I will eventually follow them up.

Many thanks, 

Eric


> On Apr 30, 2026, at 2:38, glen <[email protected]> wrote:
> 
> OK. I've done a little homework on what I'm calling your 3rd example of out 
> of equilibrium (OOE) patterns not well-classed as "evolution through 
> selection" (EtS). I watched and transcribed the Lennon talk, which was very 
> cool, particularly the sheer number of nearly inert spores in terms of 
> biomass and the energy required to produce an endospore in atp units. I can 
> use ffmpeg to extract the slides ... maybe later. Anyway, good stuff. Thanks.
> 
> But in trying to hammer out what you're gesturing at, I went a couple of 
> rounds with Claude and Asta and landed on a 5 point ball of leads, hoping 
> that listing those 5 will trigger your memory or cajole you into winnowing it 
> down to 1 thing I can do more homework on. Here's the ball. Obviously, it's 
> not the Lennon-Shoemaker cite, since you gave that one to me. But it's 
> included for completeness.
> 
> • Steven Finkel (USC): GASP/long-term stationary phase
> 
> Finkel SE. "Long-term survival during stationary phase: evolution and the 
> GASP phenotype." *Nature Reviews Microbiology* 4(2):113–120, 2006. 
> doi:10.1038/nrmicro1340. PMID 16415927.
> 
> • Zambrano & Kolter (Harvard): the GASP founding observation
> 
> Zambrano MM, Siegele DA, Almirón M, Tormo A, Kolter R. "Microbial 
> competition: *Escherichia coli* mutants that take over stationary phase 
> cultures." *Science* 259(5102):1757–1760, 1993. doi:10.1126/science.7681219. 
> PMID 7681219.
> 
> • Richard Lenski (Michigan State): LTEE
> 
> Lenski RE. "Experimental evolution and the dynamics of adaptation and genome 
> evolution in microbial populations." *ISME Journal* 11(10):2181–2194, 2017. 
> doi:10.1038/ismej.2017.69.
> 
> • Jay Lennon/William Shoemaker (Indiana → UCLA): extreme energy limitation
> 
> Shoemaker WR, Jones SE, Muscarella ME, Behringer MG, Lehmkuhl BK, Lennon JT. 
> "Microbial population dynamics and evolutionary outcomes under extreme energy 
> limitation." *PNAS* 118(33):e2101691118, 2021. doi:10.1073/pnas.2101691118.
> 
> • Cho / Palsson collaboration (KAIST + UCSD): adaptive laboratory evolution 
> of genome-reduced E. coli
> 
> Choe D, Lee JH, Yoo M, Hwang S, Sung BH, Cho S, Palsson B, Kim SC, Cho B-K. 
> "Adaptive laboratory evolution of a genome-reduced Escherichia coli." 
> Nature Communications 10:935, 2019. doi:10.1038/s41467-019-08888-6. PMID 
> 30804335.
> 
> As always, I don't intend to abuse your generosity. Feel free to ignore me. 
> The LTEE experiment is popular in the culture wars ... so I'm already 
> interested in that. >8^D
> 
> On 4/12/26 6:29 PM, Santafe wrote:
>> Sorry to drop; I also wanted to do a little looking for materials.
>>> On Apr 11, 2026, at 0:43, glen <[email protected]> wrote:
>>> 
>>> Very cool. Thanks for continuing this. I have 2 requests if you can answer 
>>> off the top of your head:
>>> 
>>> 1. One or two good citations for the 2 classes of the out of equilibrium 
>>> patterns. I'm at a loss for an example pattern Lachman might include, but 
>>> you exclude.
>> I can give you an idea how widely Michael wants to scope.  But for the 
>> example I will mention, I can’t find any publication where he built this 
>> out, or even a podcast where he discusses it.  Probably because it would be 
>> hard to find buyers.  So these are just things he used as examples in 
>> working conversations (maybe even 6 or 7 years ago now?  I’m not sure).  
>> Michael wanted to treat rocks rolling down hills at different rates as an 
>> equally good exemplar of selection.  Take lifecycles and everything 
>> biological out of the picture entirely.  This isn’t a terrible math-analogy 
>> for how mortality selection works, if we think of death as regression toward 
>> the equilibrium of a Gibbs chemical ensemble.  (In other ways, that’s a 
>> terrible mangling of categories, but for the tiny bit of math that is left 
>> in this case, it works out the same way.)  Michael’s limiting case, though, 
>> lacks any amplification step or anything like a lifecycle.  So there can’t 
>> really be anything like fecundity selection, and there isn’t persistent 
>> non-equilibrium patterning.  (One could go into the direction of erosion, 
>> and look for some kind of amplification, to produce a limited analogue to 
>> fecundity selection.  But that is still only surfing the shoulder of a 
>> transient, so it isn’t a good model for true patterned persistent states in 
>> other ways.)
>> As the other side, where there is differential amplification and 
>> attenuation, but in highly structured systems, a standard layout would be 
>> the one I always trot out by Michael Lynch, as a summary of the 
>> population-geneticsts’ abstraction:
>> The frailty of adaptive hypotheses for the origins of organismal complexity 
>> <https://linkprotect.cudasvc.com/url?a=https%3a%2f%2fwww.pnas.org%2fdoi%2f10.1073%2fpnas.0702207104&c=E,1,SEjdrDlaAVhgUCPw7DKwNWkTbJRuVRmuKU4pz59OSSsk3_oonUxuzIzs7V2wDBN4qLgnwCnjQV6Op4Y-Z3mavjH3OF1_Fbm2cbKxP8R7Bw,,&typo=1>
>> https://linkprotect.cudasvc.com/url?a=https%3a%2f%2fpnas.org&c=E,1,fjZ5phIk_IrqTJGgv17ah39fa1-Ybejc6F_QhQVELMjREITJqaRVltecU_KzmQNIvrsSIAcGY1q7dp2R_fdUqS3uql3-f5xv6rgEYMxEQw,,&typo=1
>>  
>> <https://linkprotect.cudasvc.com/url?a=https%3a%2f%2fwww.pnas.org%2fdoi%2f10.1073%2fpnas.0702207104&c=E,1,A9SMkKPecJ36LM_L4GLTmNu9FKwPliysE1va4tRSMpZ63D7ZQROFmWAszZ-QamU0ioDtjn0xf2IdFbi8Cj5fab6CKVz_i8tBZwYh9GpUDUuaMOrssZ6tsA,,&typo=1>
>>      pnas.2007.104.issue-suppl_1.cover.gif 
>> <https://linkprotect.cudasvc.com/url?a=https%3a%2f%2fwww.pnas.org%2fdoi%2f10.1073%2fpnas.0702207104&c=E,1,8A3gGNbv4ff1vr1N_zdD5r2m_RZucfXVWtzd0QbWE8csag7BBprLvlC3jZGtCxxCYW0CO5laRAWFJjoDDEqXF0M2RN6M29dkLt0_lKiiVdo5HoP4&typo=1>
>> <https://linkprotect.cudasvc.com/url?a=https%3a%2f%2fwww.pnas.org%2fdoi%2f10.1073%2fpnas.0702207104&c=E,1,zmgrLWHdvFbTlB2_-zN6U2-CqHTEDi4Rekb64e7Ha1no2l4gB316DPwrSlx939HUWtWcSzBSG2jaUxSXt_yTnNjlTPaqLeJDIWPVXtqHMfWpwiRj1io,&typo=1>
>> Now, I generally put Lynch up as a foil, because he lays out a set of 
>> systems, arguing that they are all-and-everything you need, to belittle and 
>> attack those who try to put up further “evolutionary syntheses” or their 
>> equivalent.  However, the formalisms that Lynch is actually offering only 
>> apply properly to the abstractions of the replicating genes of Williams and 
>> Dawkins.  Then, without happening to comment on the fact that he is changing 
>> the subject, he goes on to shout “of course selection takes place at the 
>> level of genotypes” etc.  Yet, where there is relational information that 
>> _makes_ genotypes genotypes, he has said nothing about the system of 
>> accounting that characterizes how such information is retained and 
>> propagated, in his earlier “all-and-everything”.  And of course, it was the 
>> wish to deal with all that relational information (and other kinds, like 
>> symbiotic dependencies in communities) that motivated a lot of the extended 
>> syntheses that he mocks and criticizes.  I do often find that his technical 
>> criticisms of the extended syntheses are appropriate, because many of them 
>> don’t seem anchored in really well-formed principles.  But to criticize the 
>> argument that something is needed seems misguided to me.  I can imagine 
>> things that go along the lines of conceptual clarity of the way Fisher 
>> worked, but that pick up the many interesting questions that were not in 
>> play in Fisher’s day.
>> I don’t know the literature on pan-genomes well, so much of what I have of 
>> them is from meetings.  I did want to mention Jay Lennon, from this meeting 
>> here:
>> Microbial communities: Energetics and dynamics across space and time 
>> <https://linkprotect.cudasvc.com/url?a=https%3a%2f%2fwww.nitmb.org%2fmicrobial-communities-workshop&c=E,1,R0Hz8SnR_Mao_B5uQ0AYJDDjNOoxBf1r9BR8Hs7yLsCtJKpl2zTtZiJWUwqhnEpyoZCubPD-Ths6yvXZOjUA-DYFnV3I6o90dqWLBplSlFWruIwmNIs-8A,,&typo=1>
>> https://linkprotect.cudasvc.com/url?a=https%3a%2f%2fnitmb.org&c=E,1,kn14GLBYf1We6T1emayQCuNYP0P9KCHKIndQDxF1WMlk8inTtcUgFnMcRugCqDk1RD_1cwYEK_bCiZxlRH_OEP-DciQ_P5b_C4lPMNdCObvuD7KZzx1rNf4,&typo=1
>>  
>> <https://linkprotect.cudasvc.com/url?a=https%3a%2f%2fwww.nitmb.org%2fmicrobial-communities-workshop&c=E,1,whd93G0RgFxHPoK7SA-OiA3LlTimIIJhzZoJwkukPGJS9zJUknTL4rSeRViFmsZ5cmctvHESEqw4NIdDQr0avqLR3uz3SDD7fjWt6e1-OSpd90YN_RAcxyPX&typo=1>
>>      95c3c6_6fcd4e52c85c426b8bc99314e9f0a8c4~mv2.png 
>> <https://linkprotect.cudasvc.com/url?a=https%3a%2f%2fwww.nitmb.org%2fmicrobial-communities-workshop&c=E,1,B6y6NRbbdeITAJeAUZMQch1oEFB8hvGznBYPalQCF0fkdieTPUy80uhpekRXc7IZBBpwUcR8xYTGsOVd14nP7p2PG77t4kpDWXk7eU2Go6NtonAHFxk,&typo=1>
>> <https://linkprotect.cudasvc.com/url?a=https%3a%2f%2fwww.nitmb.org%2fmicrobial-communities-workshop&c=E,1,O2X0qJti2YiblXCFQAyGH70Sj_9jW8M9N9ov1EGIf0U_s1p1sIFM2irYtlyFbLizwVHglJXMQ2-qZDKuLf4or7aeDgoP3TBvkibcGemdgrLdYQ,,&typo=1>
>> as someone interesting, whom I heard recently enough that I can remember the 
>> source.  I don’t have a paper that seems to exactly cover the scope of his 
>> talk, which had lots of inter-related things and off-hand comments that 
>> reflect the breadth of intuitive appreciation that a worker often has of an 
>> area, beyond what ever makes it into papers.  But, from the angle of 
>> sporulation, he does give some discussion of how dormant phases can be 
>> reservoirs of genetic capabilities, which can be actively and selectively 
>> re-activated, here:
>> pmc-card-share.jpg
>> Evolution with a seed bank: The population genetic consequences of microbial 
>> dormancy 
>> <https://linkprotect.cudasvc.com/url?a=https%3a%2f%2fpmc.ncbi.nlm.nih.gov%2farticles%2fPMC5748526%2f&c=E,1,hs8f9lgC-1OWO_1bMh5HblhkDobURbVgkAswA_GPVjzhPoExCJVXk1g86Odt55S_l61RofvaOaAcu_EIfx3mTogZ7fjh9vCThjUxzLHWXduIkwyj5FM,&typo=1>
>> https://linkprotect.cudasvc.com/url?a=https%3a%2f%2fnlm.nih.gov&c=E,1,h0fFWEpmjS7zQ2j1Zp0_WQFl1U953WMReiF6eaM0kvEeKzBDMdP5U43frE1khuFtAZPtzUdBRhQbgZ4PFQ7IP3IZmqCdlcJuU82BL7goNQ5b4V7XIPVm52Po_iEt&typo=1
>>  
>> <https://linkprotect.cudasvc.com/url?a=https%3a%2f%2fpmc.ncbi.nlm.nih.gov%2farticles%2fPMC5748526%2f&c=E,1,D_d3wMDx5uEwQvw3lH4hHYNT_euFKRYu6TeVTfhm0VdRPgXg_6k8B8Db5TXii9aE3N88JsZG6_qiY4ZUXgShUkU0FT-Zri3daGV7y7Lc_627IiL8NOs_4GJr-w-q&typo=1>
>> <https://linkprotect.cudasvc.com/url?a=https%3a%2f%2fpmc.ncbi.nlm.nih.gov%2farticles%2fPMC5748526%2f&c=E,1,lAscp8Q6fxK2TjRnjRJIKXnaGw7JqyN0u9-wPU4qaWI2Ls40q7S5YkZ6e0knPyW0rdx5dMXa7YweRerDckHwsrm7mpFaPVIvYwf-uh0Rq_5St3u2VPwZ1uQT1MIa&typo=1>
>> Somebody else, who does very-long-term starvation phenotypes on E. coli, and 
>> shows that the whole genome and cell form undergo radical metamorphoses, was 
>> the first person who really got my attention on the dynamic and intentional 
>> characteristics of pan-genomes.  But I don’t remember who it was.  (Oddly, I 
>> have some synesthetic image of the room I was sitting in watching, but I 
>> couldn’t tell you what meeting or what year it was in.)  He is somebody 
>> well-known for this.
>>> 2. I'm assuming you and Lachman's ability to grok and play along with each 
>>> others' preferences is *because* you work in the same physical location and 
>>> can talk informally back and forth. Is that true? Or do you think you could 
>>> come to the same facile donning-doffing of each perspective if you *only* 
>>> communicated by electronic means ... or through publication letters and 
>>> such?
>> It’s a good question.  Probably equal amounts of both.
>> My impulse — being someone given to abstraction — is to suggest that the 
>> main driver is temperament.  Neither Michael nor I is out to capture or 
>> defend territory.  We also share taking no enjoyment in “conversations” that 
>> go in circles forever because the interlocutors talk past each other and 
>> misunderstand each other’s claims.  Michael is, in general, a much more 
>> easy-going and tolerant person than I am, so he doesn’t tend to the 
>> immediate impatience and annoyance with such conversations that I have.  But 
>> he never drifts into that direction, so there is never needless upstream 
>> swimming to do.  He is also very clear with his categories.  Since we both 
>> enjoy and are looking for questions that are actually about something, then, 
>> it is almost-always pretty systematic to see where a misunderstanding has 
>> happened, and figure out how to unravel it to get to a meaningful question 
>> we can try to puzzle out.
>> But equally much, being in a room has mattered.  For a long time now, it has 
>> been several years at a time between my path-crossings with Michael.  
>> However, it does turn out to be invaluable that I can trudge a half-hour 
>> across town in the snow, to sit for an afternoon in a room with him, to try 
>> to hash through something.  The counterexample that shows this is probably 
>> essential is that he makes certain statements to the effect that Hector 
>> Zenil’s information-theoretic criticisms of Walker and Cronin’s Assembly 
>> Theory are “wrong”.  While there is a lot of Zenil’s screed in his blog 
>> posts that is unhelpul — but which reviewers and editors were largely able 
>> to get him to cut out when he got a few papers on this published — there is 
>> a core of his assertion, that the Assembly Index is a certain version of a 
>> compression index, that seems correct to me.  I am sure that Michael speaks 
>> in good faith, and also that he knows what he is talking about.  And I am a 
>> semi-tourist in these algorithmic information things, not an essential 
>> worker.  But for all that, I don’t understand just what Michael is claiming 
>> in detail, and probably won’t until I have a couple hours with him for which 
>> that is the main topic to sort out.  I have felt the lack of that as a kind 
>> of exposure, because I worry where I am missing something.
>> It’s all interesting,
>> Eric
> 
> 
> -- 
> ¡sıɹƎ ןıɐH ⊥ ɐןןǝdoɹ ǝ uǝןƃ
> ὅτε oi μὲν ἄλλοι κύνες τοὺς ἐχϑροὺς δάκνουσιν, ἐγὰ δὲ τοὺς φίλους, ἵνα σώσω.
> 
WEBVTT

00:00.000 --> 00:07.000
Good afternoon, everyone. I can start off by challenging some assumptions, I guess,

00:07.000 --> 00:15.000
about the physiology of microbial systems and start with the proposition that most organisms,

00:15.000 --> 00:21.000
microbes included, but also plants and animals, live in environments that are typically not

00:21.000 --> 00:27.000
suitable for growth and reproduction, at least not maximal growth and reproduction. And as

00:27.000 --> 00:31.000
a result of that, those populations are at risk for extinction. But a lot of different

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strategies have evolved among diverse organisms, including their ability to alter their behaviors.

00:38.000 --> 00:43.000
Some organisms will disperse into new environments and take on the risk of encountering some

00:43.000 --> 00:48.000
new set of environmental conditions that might be better. Or some organisms may choose to

00:48.000 --> 00:54.000
just stay put and evolve locally through a process of natural selection and local adaptations

00:54.000 --> 01:00.000
to those model conditions. Another option, however, that I'm going to talk about today

01:00.000 --> 01:07.000
is that organisms can disperse in time. So many organisms have all the capacity to engage

01:07.000 --> 01:13.000
in dormancy, which we're going to define as the ability for an individual to enter a reversible

01:13.000 --> 01:20.000
state of reduced metabolic activity. And that's a pretty loose definition, but when we do

01:20.000 --> 01:27.000
that, there are many different types of plants and animals, bacteria, fungi, insects, rotifers,

01:27.000 --> 01:33.000
protists, amphibians, birds, all different types of organisms have this ability to engage

01:33.000 --> 01:38.000
in this process of dormancy. And so that's an example of convergent evolution, because

01:38.000 --> 01:43.000
the way in which those processes have evolved has arisen independently. There's no shared

01:43.000 --> 01:49.000
origin in their ability to achieve this process. So it kind of suggests that there's a solution

01:49.000 --> 01:56.000
to some kind of common problem that isn't encountered. And I guess I want to say by

01:56.000 --> 02:02.000
showing these different examples, also highlight the mechanisms by which organisms can. For

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some, it's a very passive process where an individual can just kind of passively fall

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into a state of inactivity. But in many instances, there's really complex underlying mechanisms

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that control the ability of an organism to engage in this life history process. Different

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pathways, different developmental pathways, different genetic regulatory mechanisms, often

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leading to vastly different changes in organismal morphology as it goes from a state of being

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an actively growing organism to one that's metabolically connected.

02:38.000 --> 02:43.000
So despite all those fascinating details, I'd like to argue that there maybe are just

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some three essential criteria that need to be met in order for an individual, regardless

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of what taxonomic group you're thinking about, to engage in this process. The first thing

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is that an individual needs to be able to occupy at least one of two different states.

02:59.000 --> 03:04.000
In the most simplest version of dormancy, you could have an on versus off metabolic

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state. Criterion two is that individual then needs to be able to move or transition between

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those two states. And that can happen in different ways. So we heard a little bit about this

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idea of stochastic switching so that environments may be so unpredictable that individuals would

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randomly move between an active and inactive state. But in many cases, they're tracking

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environmental cues and that's what's regulating the transitions between those two metabolic

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states. So it could be temperature, it could be a depletion of resources, the accumulation

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of waste products in the environment, all those occurring perhaps at the local patch

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scale, or individuals can be queuing in on broader geographic cues like changes in photo

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periods from here. The third criteria that must be met is that there's no benefit to

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be dormant because you're not reproducing. And that's ultimately what's important and

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selected for by natural selection. But you can enjoy protection against the environmental

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conditions that would otherwise increase your mortality. So there has to be some protection

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that's afforded to individuals that are not engaging in metabolism and replication. So

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those are the central criteria for being a dormant order and engaging in this process.

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So we've been thinking about these processes and how they influence microbial communities

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for quite a while now. I think we've been able to demonstrate that it's important for

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the maintenance of the diversity of complex microbial communities, and in some case helps

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us understand and predict the functioning of an ecosystem. And the figure I'm showing

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here right now is just looking at the accumulation of metabolically inactive individuals into

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all microorganisms. And so what you can see is that they're accumulating collectively

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the abundance and biomass of these different individuals in different ecosystems in a variable

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way. In some cases, in soil, which we care about in terms of thinking about the sequestration

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of carbon from the atmosphere, nutrient cycling for crop and food production, upwards of 90%

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or more of those microbial cells are in a state of metabolic inactivity. And so these

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observations that we made a long time ago, just by combing information from the literature,

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motivated us to be thinking about developing experimental systems that we can bring into

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the lab to generate and test theory regarding the evolutionary properties of microbial life.

05:25.000 --> 05:36.000
Yeah, so in this case, this is all based on single cell data where you could look at,

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for example, the recovery of ribosomes from cells or the ability of certain metabolic

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dyes that will fluoresce in a certain way if there's an active electron transport chain.

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And we're looking at, we're classifying those either after or in the next.

06:01.000 --> 06:05.000
Yeah, that's a good question. So the residence time of the ecosystem is really important.

06:05.000 --> 06:09.000
If you're not replicating, if you think about a chemostat and you put a bunch of cells in

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there and they go dormant, then they're just essentially inert particles that we would

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So it must mean that the human gut or the animal gut is kind of deviating in some way

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from first order expectations of something like a chemostat. There are lots of folds

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and villi and things and pockets and ducts that can trap microbiota from the gut and

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probably reduce residence time.

06:38.000 --> 06:40.000
Yeah, those are all surface water samples.

06:43.000 --> 06:51.000
So I'm just curious that the idea of this kind of binary decision between either being

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growing or not growing, I guess in principle some forms of, that's a wooden performance

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you could just be up on an end of a continuous gradient. Like, so I invest more in RPOS,

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but that slows my growth. I'm just wondering, like, how many of these cells that are active

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are at a lower activity level than they could in principle accidentally achieve in those conditions?

07:16.000 --> 07:20.000
Yeah, I think the idea that there could be some kind of binomial distribution of metabolic

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activity in a microbial community is something that we've recently kind of dismissed and

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or ruled out. It seems like there is more of a continuous distribution such that there

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is a small proportion of cells that are carrying out most of the activity and there's these

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long term distributions of metabolic and kinetics. But it's not two distinct distributions.

07:45.000 --> 07:52.000
So yeah, so we wanted to develop an experimental system that we could work with in the laboratory

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and address some questions. And for a long time I avoided the temptation and suggestions

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that we should be working with SCORE coming back to this. Mostly because I think there

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are organisms that don't do sporulation. I was initially a little bit reluctant to accept

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that this was the model. But then I realized that there were a lot of features to study

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SCORE forming bacteria regarding their genetics, their ability to be visualized, experimental

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trafficability in general. And so this is a really ancient form of a dormancy. It's

08:26.000 --> 08:31.000
only found within one phylum of bacteria. For those of you who are not microbial biologists

08:31.000 --> 08:36.000
or not familiar with the tecton and phylogeny, there's hundreds of different phylum. We

08:36.000 --> 08:42.000
are one phylum, a chordata, a little chord, basically every other organism that walks

08:42.000 --> 08:48.000
on the lens or tube. So there's only one phylum of bacteria in the tree of life, called the

08:48.000 --> 08:53.000
bacillota from accutes. And even within that lineage, not all organisms do that. But the

08:53.000 --> 09:00.000
ancestor that is at the root of that tree was a SCORE forming, had the SCORE forming

09:00.000 --> 09:05.000
capacity. And that dates back to about 3 billion years. So this is a really ancient trait.

09:05.000 --> 09:11.000
It's also very complex. There are upwards of 500 genes that are required and they're

09:11.000 --> 09:15.000
upregulated when a cell goes from growing under good condition, where an individual

09:15.000 --> 09:21.000
can divide once every 20 minutes, to entering into this pathway where you upregulate tons

09:21.000 --> 09:28.000
of genes to make SCORE. It's also very timely, time consuming. So again, 20 minutes. To carry

09:28.000 --> 09:35.000
out the whole process to create a mature SCORE takes about 8 hours. But when you're done,

09:35.000 --> 09:43.000
you have a structure that is extremely hardy. It's almost energetically inert. You can expose

09:43.000 --> 09:47.000
it to any kind of environmental condition you can think of and the cells usually survive.

09:47.000 --> 09:52.000
People put them on the outside of the International Space Station in the vacuum of space and they

09:52.000 --> 09:58.000
seem to survive those conditions just now. And as a result of that, they have a pretty

09:58.000 --> 10:02.000
wide geographic distribution. You can find endoscores virtually everywhere. They're littered

10:02.000 --> 10:07.000
across soils, they're found in our guts, they're found in the oceans, where it's been conservatively

10:07.000 --> 10:11.000
estimated that there are somewhere on the order of 10 to the power of 28 endoscores.

10:11.000 --> 10:17.000
And so if we use numbers that people have, thinking about global patterns of diversity

10:17.000 --> 10:23.000
and abundance, there's about 10 to the 30 cells, 10 to the 29 to 30 microbial cells

10:23.000 --> 10:28.000
from the planet. So just with this one group of organisms, we can conservatively conclude

10:28.000 --> 10:34.000
that about 10% of the global microbial biosphere is in a seed bank or is in some state of the

10:34.000 --> 10:45.000
environment. So I think this all kind of sets up a bit of an energetic paradox or a

10:45.000 --> 10:51.000
conundrum, at least for me, because these spores and the production of this pathway,

10:51.000 --> 10:56.000
which is time consuming and energy consuming, only happens when there's vanishingly small

10:56.000 --> 11:01.000
quantities of energy in the surrounding environment. So why would you go through this whole process

11:01.000 --> 11:07.000
of going through this elaborate process of up-regulating all these genes and making proteins

11:07.000 --> 11:13.000
to create this protein-rich complex structure when there's no energy around in the environment?

11:13.000 --> 11:19.000
And so this kind of just sort of begs the question in an unknown, which is what is the

11:19.000 --> 11:26.000
energetic cost of making an endoscore? And the approach to do this is what we thought

11:26.000 --> 11:30.000
about for a while. You could imagine that there are microcell limits in me and other

11:30.000 --> 11:35.000
types of approaches where you can carefully measure the amount of energy flux in a cell,

11:35.000 --> 11:41.000
and people have tried that without much success. We adopted another strategy that was developed

11:41.000 --> 11:47.000
by a colleague of mine, Mike Lynch, about 10 years ago, where he took a bottom-up approach.

11:47.000 --> 11:54.000
And initially it was used to quantify the cost of making a gene in units of ATP, which

11:54.000 --> 12:00.000
is a universal currency of life. Since then, that process has been extended to quantify

12:00.000 --> 12:05.000
the energy involved in making new membranes. It's been used to quantify the energetic

12:05.000 --> 12:10.000
cost of making entire viruses. And it's been recently used to estimate the cost of producing

12:10.000 --> 12:17.000
and making an entire multicellular metadome, all by based on the assumptions of the cost

12:17.000 --> 12:22.000
of making a nucleotide or a ribonucleotide, and then translating that information into

12:22.000 --> 12:26.000
protein. Those are the three dominant costs. There's other things that are going on that

12:26.000 --> 12:32.000
we can account for, but those are the three major sources of energy consumption in ATP

12:32.000 --> 12:39.000
for biosynthesis. So this work is all being conducted by a former postdoc of mine, John

12:39.000 --> 12:49.000
Impelli, a former Ph.D. student at Washington University.

12:49.000 --> 12:56.000
So we use this approach. Basically, it's just a detailed countdown. It's not really all

12:56.000 --> 13:01.000
that exciting. You know which genes in a genome are associated with the process of making

13:01.000 --> 13:06.000
a score, and you count those up. You know which ones are being transcribed by mining

13:06.000 --> 13:11.000
and existing transcriptome datasets that are being done at precise time resolutions. And

13:11.000 --> 13:15.000
there are databases where people have measured protein expression under those same conditions

13:15.000 --> 13:22.000
under these characteristic stages of development. And so the first thing that's interesting

13:22.000 --> 13:26.000
that the cell needs to do when it engages in the process of correlation is it makes

13:26.000 --> 13:33.000
a copy of its genome. So there's now two copies. And shortly thereafter, you get the formation

13:33.000 --> 13:45.000
of a septum. To the left of that, you have a larger mother cell, and to the right of

13:45.000 --> 13:49.000
that, you have the developing core cell. There's going to be one copy of the genome on the

13:49.000 --> 13:53.000
left side, and there's going to be another copy of the genome on the right side. After

13:53.000 --> 13:58.000
that, it's been set up. Now you have differential gene expression occurring on both sides of

13:58.000 --> 14:03.000
that barrier, and there is some exchange that's going on between the two of them. Eventually,

14:03.000 --> 14:07.000
there's a score that starts to develop. It engulfs the mother, and you result in the

14:07.000 --> 14:14.000
end with a free-standing mature endosport. This whole investment is extremely front-loaded

14:14.000 --> 14:19.000
based on the data that we've estimated. So in the first two hours of this eight-hour

14:19.000 --> 14:25.000
process, 85% of the ATP investment occurs. And it's sort of coincidental or not that

14:25.000 --> 14:30.000
this happens right before this dashed vertical line, which is the point of commitment or

14:30.000 --> 14:35.000
no return. Once you get beyond that point, the cell can no longer change its mind and

14:35.000 --> 14:40.000
go back to being a vegetative cell. So there's a decision that needs to be made with consequences

14:40.000 --> 14:45.000
for the recuperation of allocated energy, whether it's opportunity costs where energy

14:45.000 --> 14:50.000
and ATP can be used for other processes that might be generating energy and involved in

14:50.000 --> 14:54.000
other processes beyond dormancy.

14:54.000 --> 14:55.000
Yeah.

14:55.000 --> 15:02.000
How big is the exchange rate investment compared with the COVID-19 sales for experiential

15:02.000 --> 15:03.000
environment sales?

15:03.000 --> 15:07.000
So that's a great question. And if I can just pause for one second, I'll get to that because

15:07.000 --> 15:12.000
I have the same exact... What's the exchange rate or currency? I don't know how to interpret

15:12.000 --> 15:17.000
the nine ATPs compared to other cellular processes. So I'm going to have a figure where I go through

15:17.000 --> 15:22.000
and show that.

15:22.000 --> 15:31.000
Should we think of this as having accepted the ordinary life cycle reproductive system

15:31.000 --> 15:37.000
or is it something completely independent that is going to parallel in place?

15:37.000 --> 15:46.000
They're distinct. Yeah. There's a decision that's made and once they undergo that process,

15:46.000 --> 15:51.000
cells are no longer going under any kind of vegetative growth. So there's two distinct

15:51.000 --> 15:55.000
choices and bifurcations in there.

15:55.000 --> 16:02.000
Even the chromosome copy, is that using standard machinery and then stream some other choices

16:02.000 --> 16:03.000
maybe?

16:03.000 --> 16:06.000
Yeah. And it happens very early on. And so even if the cell were to proceed with vegetative

16:06.000 --> 16:11.000
growth, we'd still need to make a copy of its genome. But early on in the stages of

16:11.000 --> 16:16.000
spore relation, we need to have a second copy made and then there's chromosomal segregation

16:16.000 --> 16:26.000
into the development of the score.

16:26.000 --> 16:30.000
So translation costs dominate this. So genome replication that we're talking about right

16:30.000 --> 16:37.000
now is important, but it's not the predominant cost. Making proteins is the biggest thing.

16:38.000 --> 16:43.000
Thinking about this subcellular allocation strategy, there's analogies to thinking about

16:43.000 --> 16:47.000
embryogenesis and the way in which maternal investments in their offspring and we see

16:47.000 --> 16:51.000
parallels to that here. The mother cell is accounting for a disproportionate cost of

16:51.000 --> 16:58.000
the spore development. She's paying 90% of the total process of making a spore is occurring

16:58.000 --> 17:09.000
in that left-hand side of the middle cell.

17:09.000 --> 17:13.000
So what I showed you in the last process, early on there was a diagram showing the transition

17:13.000 --> 17:19.000
into dormancy and out of dormancy. So this is the cost of initiating dormancy. What I

17:19.000 --> 17:27.000
want to say is that if you stay as a dormant spore for 100,000 years, which one of my undergraduates

17:27.000 --> 17:33.000
now is resurrecting cells from ancient Vietnamese settlements and it seems to be pretty easy

17:33.000 --> 17:39.000
to do, if they stay in that state eternally, then there's no distinction between that being

17:39.000 --> 17:45.000
a potentially viable cell and a dead cell. In order for this to be an evolutionarily

17:45.000 --> 17:50.000
advantageous strategy, the spore needs to germinate, it needs to wake up, it needs to

17:50.000 --> 17:55.000
outgrow, and it needs to divide. And if that doesn't happen, then all of the investments

17:55.000 --> 18:00.000
of ATP up to that point are for naught. So what we wanted to do was come up with a full

18:00.000 --> 18:05.000
cost accounting of this entire life cycle, so we're also quantifying the costs associated

18:05.000 --> 18:11.000
with revival. And this happens over a much shorter time scale, so our intuition, naively,

18:11.000 --> 18:15.000
was that this should be a less costly process. In fact, what we found is that revival is

18:15.000 --> 18:23.000
more expensive than the initiation of formation. And that's probably due, again in retrospect,

18:23.000 --> 18:30.000
again to proteins, right? So transcripts of proteins are about 100 to 1,000 fold more

18:30.000 --> 18:37.000
abundant inside a cell than they are in transcripts. And this spore needs to, as it's outgrowing,

18:37.000 --> 18:43.000
needs to produce a vast repertoire of proteins that are needed for vegetative growth. And

18:43.000 --> 18:48.000
so there's a complete proteome turnover, and that seems to be why we're seeing a large

18:48.000 --> 18:54.000
decline associated with spore revival in general. And so how do they do this? It's

18:54.000 --> 18:59.000
not relying on the storage of internal ATP reserves, but these ATP surveys are certain

18:59.000 --> 19:05.000
of that. In the literature, we've done some careful investigation, and there's at most

19:05.000 --> 19:12.000
a couple hundred ATP molecules inside of an under-spore. So that must be enough to reboot

19:12.000 --> 19:17.000
a spore, but it's definitely not enough to meet a great shortfall by at least six orders

19:17.000 --> 19:24.000
of magnitude, and what's required for that under-spore to rebar. Which means, I think,

19:24.000 --> 19:29.000
that germinating an under-spore has to make the timing really important, because as soon

19:29.000 --> 19:34.000
as it germinates, it needs to get its hands on a sufficient supply of exogenous resources

19:34.000 --> 19:39.000
from outside the cell to meet a solid germination. Again, otherwise, the spore, the whole spore

19:39.000 --> 19:42.000
cycle will come to a close.

19:42.000 --> 19:48.000
So do you have any direct understanding of the degradation of proteins, the degradation

19:48.000 --> 19:54.000
flux of these things? There's this proposal of that. Sometimes it costs four ATP per amino

19:54.000 --> 19:57.000
acid to do preparation, but sometimes you can actually get energy from that process.

19:57.000 --> 20:03.000
Yeah, and I think there is some internal recycling. So we have kind of worked through this, and

20:03.000 --> 20:07.000
there's a manuscript that we can develop, and there are some calculations that might

20:07.000 --> 20:11.000
diminish some of that cost, and there's some internal recycling during the hydrolysis process

20:11.000 --> 20:19.000
associated with germination. But I don't have those numbers.

20:19.000 --> 20:27.000
Okay, so getting back to this question of how do we compare a process or a relative

20:27.000 --> 20:35.000
option, these costs, to other things that a bacillus cell might do. And so we carried

20:35.000 --> 20:39.000
out the same process, not just with sporulation and germination, but a whole bunch of other

20:39.000 --> 20:44.000
things that this cell does using data that we can get our hands on. And from that, we

20:44.000 --> 20:48.000
found that sporulation is probably one of the more expensive things that a cell can

20:48.000 --> 20:54.000
do. It makes up about 10 percent of the total budget of the cell. And there are a bunch

20:54.000 --> 20:59.000
of alternate strategies that these cells would prefer to engage in when confronted with stress

20:59.000 --> 21:05.000
that they do before they will produce an endosporin. So some of them, when stressed, will start

21:05.000 --> 21:12.000
to collectively engage in biofilm formation. They engage in things like cannibalism. They

21:12.000 --> 21:19.000
start expressing competence. They allow them to acquire genes from their environment, which

21:19.000 --> 21:23.000
perhaps could influence their fitness. There are a bunch of alternate strategies. All of

21:23.000 --> 21:28.000
those are much less expensive than making an endosporin.

21:28.000 --> 21:34.000
So at the end, there's a question about the break-even point here. And so let's imagine

21:34.000 --> 21:41.000
that you can reduce maintenance energy requirements by 100,000. So that's a cost that you have

21:41.000 --> 21:45.000
to pay continuously, but that might still be advantageous compared to the one-time big

21:45.000 --> 21:52.000
investment of making a score. And so the characteristic time or frequency at which fluctuations must

21:52.000 --> 21:57.000
occur between good and bad environments in order for sporulation to be optimal for this

21:57.000 --> 22:03.000
to be the favored, persistent strategy is about 30 days. So once the environment goes

22:03.000 --> 22:09.000
beyond being inhospitable for growth and reproduction, once you get to that 30-day

22:09.000 --> 22:14.000
point, now sporulation starts being a beneficial process.

22:14.000 --> 22:18.000
I see that we're standing here, so I'm going to just wrap up. We thought a little bit about

22:18.000 --> 22:22.000
how this could limit something called sporulation efficiency. If you put cells in a given environment

22:22.000 --> 22:27.000
that's not suitable for growth and reproduction, which fraction of those cells will be able

22:27.000 --> 22:33.000
to be producing endospores, we see in the literature it ranges from 0 to 100 percent

22:33.000 --> 22:38.000
and with a mean of about 30. This has commonly been in bulk as a form of bet hedging that

22:38.000 --> 22:43.000
not all individuals need to do this process to ensure the persistence of this sporulation.

22:43.000 --> 22:48.000
We don't acknowledge to us that actually it seems that there's constraints and energy

22:48.000 --> 22:53.000
limitation at the population scale that prevents cells from being able to form endospores.

22:53.000 --> 22:57.000
And the last thing I wanted to talk about, and I won't go into a ton of detail here,

22:57.000 --> 23:01.000
is the evolutionary implications for cost and the maintenance of this trait over long

23:01.000 --> 23:05.000
periods of time. I mentioned it was first evolved three billion years ago. This trait

23:05.000 --> 23:12.000
has been lost repeatedly over geologic time scales. And in addition, if you passage these

23:12.000 --> 23:16.000
cells in the laboratory, if I put them in a cleanest cell, if I put them in batch culture

23:16.000 --> 23:20.000
and I passage them under good conditions, in a matter of weeks, months, we see a three

23:20.000 --> 23:25.000
billion year old trait. You go, why is that? Because five to ten percent of the entire

23:25.000 --> 23:30.000
genome is devoted to sporulation. And when that's under relaxed selection, it's a large

23:30.000 --> 23:35.000
target for mutation to accumulate. Essential genes that once perturbed, you've lost that

23:35.000 --> 23:42.000
trait in perpetuity. So this is the use it or lose it idea that under relaxed selection,

23:42.000 --> 23:48.000
not knowing anything about energetics, we see the loss of this trait over geologic time

23:48.000 --> 23:53.000
scales. We did some work with mutation accumulation experiments, which allowed us to look at deletions,

23:53.000 --> 23:59.000
so large traits of DNA that can be lost. And this would be an energy-saving mechanism that

23:59.000 --> 24:04.000
is consistent with adaptive streamlining, so why genomes get small. So if evolution

24:04.000 --> 24:09.000
can see those nucleotides that are being paved through the process of genome duplication,

24:09.000 --> 24:13.000
selection can actually move them in a way that saves energy for the cell, becomes the

24:13.000 --> 24:20.000
consequence of losing this trait. And so I think some of these things could be important

24:20.000 --> 24:24.000
for thinking about community dynamics, which has been a theme of what we've been talking

24:24.000 --> 24:29.000
about. Some of the work that we're doing is trying to think about how spores can provide

24:29.000 --> 24:32.000
defense against phages, and that seems to be something that we're going to hear about

24:32.000 --> 24:38.000
tomorrow. They can't attach to the receptors, because there aren't any receptors on these

24:38.000 --> 24:44.000
spores. And so there is a physical defense that is important for phage attack, and subsequent

24:44.000 --> 24:51.000
rates of coevolution and diversification. So thinking about this as a mechanism of abiotic

24:51.000 --> 24:55.000
tolerance, there's implications for thinking about the diversity of biological systems.

24:55.000 --> 24:57.000
Okay, thank you.

24:57.000 --> 25:05.000
I have time for a few questions.

25:05.000 --> 25:30.000
Great talk. I was wondering about the 180Ps that you mentioned. Do you think they are

25:30.000 --> 25:34.000
not getting hydrolyzed, or are they getting constantly generated? In other words, is it

25:34.000 --> 25:40.000
a non-occurring, stationary-stating thing, or is it a turnover of ATP in the spore?

25:40.000 --> 25:45.000
From people I talk to, and people who study ribosomes and other cellular processes, it's

25:45.000 --> 25:51.000
a very hard thing to study and to measure. My expectation is that of any form of dormancy

25:51.000 --> 25:57.000
that I'm aware of, spore is the least amount of biological activity in a turnover. So perhaps

25:57.000 --> 26:01.000
there's actually consumption of ATP over time, but I don't think there's any generation of

26:01.000 --> 26:05.000
new ATP in the endosporus.

26:05.000 --> 26:27.000
Could you contrast the state of being dormant versus being an endosporus and develop the

26:27.000 --> 26:31.000
frequency at which one finds these two states in nature?

26:31.000 --> 26:36.000
I'm very careful in how I define dormancy, and I keep it super generic, because there's

26:36.000 --> 26:41.000
a lot of language to describe different ways in which organisms achieve the same thing.

26:41.000 --> 26:45.000
I think those differences are interesting and important. I would definitely say that

26:45.000 --> 26:50.000
endosporus is a classic example of dormancy. I'm not sure there being any other organism

26:50.000 --> 26:58.000
that would be more metabolically inactive than an endosporus. I'm not sure if that's

26:58.000 --> 27:02.000
your question, but...

27:02.000 --> 27:07.000
My question is, I just think that you refer to all the time that this is dormant. It's

27:07.000 --> 27:09.000
a wider classification.

27:09.000 --> 27:10.000
Wider?

27:10.000 --> 27:14.000
That's my guess. I don't know yet. Endosporus is dormant.

27:14.000 --> 27:15.000
For sure.

27:15.000 --> 27:22.000
Okay. I just don't know.

27:22.000 --> 27:24.000
It only occurs in one phylum.

27:25.000 --> 27:31.000
This particular flavor of dormancy only occurs in a subset of bacteria that fall within one

27:31.000 --> 27:32.000
phylum?

27:32.000 --> 27:36.000
Yes, it must be. Other phylum must have it.

27:36.000 --> 27:42.000
They do a different one, right? Maybe not to the same degree. Again, this is an example

27:42.000 --> 27:47.000
of a really complex form of dormancy. They're exceptionally long-lived compared to other

27:48.000 --> 27:55.000
One last question from Alfred.

27:55.000 --> 28:04.000
Yeah, very nice analysis. I really like this. Ten percent of the total energy budget for

28:04.000 --> 28:12.000
stolomation is not that bad. From your curve, it looks like the biggest energy expense is

28:12.000 --> 28:22.000
for the checkpoint. How much energy, in terms of metabolizing per unit time, or how much

28:22.000 --> 28:30.000
metabolism would need to go on to cover the last hum? And also, obviously, the cells cannot

28:30.000 --> 28:39.000
predict the environment and whether the snacks will be. Are there any ideas of what the selection

28:39.000 --> 28:44.000
is behind that, or is it simply those that can't make it, you don't have a file in this

28:44.000 --> 28:45.000
environment?

28:45.000 --> 28:51.000
I mean, some element of this is work hypotheses necessarily going in about the checkpoints,

28:51.000 --> 28:55.000
but we knew that those checkpoints existed, and it just so happens that a lot of the energy

28:55.000 --> 29:01.000
was expanded prior to that. If conditions change in that two-hour window before commitment,

29:01.000 --> 29:05.000
then the cell has an opportunity to reuse the energy that's been collected for other

29:05.000 --> 29:09.000
purposes. Once you get past that, that's the point of no return, and there's no way

29:09.000 --> 29:15.000
to recoup that energy unless you go all the way through the process of making a mature

29:15.000 --> 29:22.000
stool and then successfully germinate and outgrow. So, I'm not sure what happened after

29:22.000 --> 29:26.000
the checkpoint, but it looks like there's not as much in terms of energy as premature.

29:26.000 --> 29:31.000
It's just really 85 percent of it is in that first two hours leading up to the formation

29:31.000 --> 29:33.000
of the cell.

29:33.000 --> 29:40.000
And how much longer could the cell live with this 85 percent in terms of maintenance energy?

29:40.000 --> 29:42.000
I mean, how much mileage does it require?

29:42.000 --> 29:44.000
What could you do with that 85 percent?

29:44.000 --> 29:45.000
Right.

29:45.000 --> 29:50.000
Yeah, yeah. Let's probably go back to that table where I showed a comparative cost, and

29:50.000 --> 29:56.000
maybe you could make a bioform, or maybe you could express some compositions, or make

29:56.000 --> 30:02.000
up 75 percent in maintenance metabolism for that period of time. You could put in those

30:03.000 --> 30:04.000
Thank you.

30:04.000 --> 30:05.000
Somebody's over making bricks.

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