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Purely “Lamarckian” evolution?

Yup, I really wrote that.  In a lab so strongly influenced by Darwin, I just invoked the name of Lamarck, who is often framed as the anti-Darwin. In no way am I defending any aspect of Lamarck’s support of the “Great chain of being” to describe the
(super)natural progression of organisms through time. Rather, I am invoking the evolution based upon acquired phenotypes. This has been rightly dismissed as being able to describe any broad timescale of evolution, but what about the potential role for epigenetics? Might anything here be considered evolution?

Late in 2019, a paper from our lab championed by Jessica Lee and co-first author Siavash Riazi describes how Jessica discovered that phenotypic variation can permit a population  of Methylobacterium extorquens to survive an otherwise lethal formaldehyde stress (PLOS Genetics, 2019. 15:e1008458).

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Jessica found that the rare survivors were phenotypic variants (no mutations anywhere), supported by several methods including excellent video microscopy data (below) from Shahla Nemati in the lab of Andreas Vasdekis here at University of Idaho (who recently was promoted to Associate Professor in Physics, woo hoo!). Rather than having a population of discrete populations of highly tolerant and weakly tolerant cells (akin to antibiotic persistence), Jessica found that the concentration that cells could survive was a wide, dynamic continuum.Screen Shot 2020-04-10 at 5.02.46 PM.png

Siavash led our effort to model how this distribution of tolerance changes in different environments in terms of growth, death, and transitioning across a continuous scale of formaldehyde tolerance. Working with co-advisor Chris Remien, Ben Ridenhour, Jessica, and myself, he was able to develop a simple PDE that allows us to conclude, amongst other things, that formaldehyde tolerance is inherited over a large number of generations. Finally, Jessica and Jannell Bazurto analyzed RNA-Seq data to determine that these phenotypically tolerant cells have a distinct transcriptome from either low tolerant cells or the immediate stress response of low tolerance cells to formaldehyde exposure.

All told, we observe selection upon phenotypes that show a fair amount of phenotypic inheritance: all the ingredients that define evolution. No allele changes were observed, but the distribution of inherited phenotypes did change. As a visual metaphor, I discussed this scenario with visual artist Cody Muir, who was at IBEST, and this resulted in a fun visual that mixes seeing only some colonies grow with the Lamarckian metaphor of the giraffe’s neck:

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Moving forward, we look forward to uncovering the physiological basis of phenotypic heterogeneity/inheritance, as well as beginning to look at how Lamarckian and Darwinian processes can jointly influence evolutionary outcomes.

We’ve welcomed a number of new lab members in the past months

It has been a pleasure to bring some new faces into the lab over the past months. Olivia Speare – now Olivia Benski – has transitioned from an undergrad to a technician working on our EPSCoR project with Tomislav. Monica Pedroni has joined us a second lab technician, and has been working with Sergey on both our NSF Dimensions of Biodiversity project and our DOE Biosystems one. Cole Garrett and Drew Johnson are both doing undergrad research in the lab, Cole with Sergey looking at PHB accumulation and Drew with Tomislav looking at evolution of growth on methoxylated aromatics. Giovanna Girolami has joined us as an UG tech making media, doing sterilization, etc. And since the last such post, we have had Mete Yuksel, Hannah Ringel, and Maria Elizarraras join the lab and then move on to other opportunities.

Sergey and I wrote a Preview for Cell paper on defining microbial populations

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In the morass of metagenomic sequence data on microbes, it is unclear what a unit should even be in a community. Ideally, one would want to uncover the core populations present: the set of strains that actually are exchanging genetic information and are reasonably cohesive, even in the presence of a degree of input from outside sources. The Polz lab has put forward a fantastic new method in Arevalo et al. “A reverse ecology approach based on a biological definition of microbial populations” (Cell, 2019. 178:820-834). for doing so that is based upon the simple concept that the length distribution of perfectly matching sequences can serve as a chronometer of separation. In the absence of exchange, two lineages emerging from the same genome sequence will ultimately accumulate random differences that will leave behind an exponential distribution of perfect sequence matches. If they continue to exchange, however, this will lead to an excess of longer sequence matches than expected. Indeed, this pattern is seen amongst strains previously identified as being of the same population. Furthermore, there is the substantial advantage that it identifies precisely which genes are being exchanged, thereby providing clues as to the success of one population versus each other, hence the concept of a “reverse” approach to ecology.

In our Preview – “Align to define: ecologically meaningful populations from genomes” (Cell, 2019. 178:767-768) – Sergey Stolyar, a Research Associate Professor working with my group, and I point out how these units defined upon exchange are actually narrower than “exact sequence variants” (ESVs), which have already been thought of as too narrow by some. We point out that the ecological distinctiveness of lineages in lab-based experimental evolution is often but one or a few mutations, so this seems quite consonant with their findings. It remains unclear whether these populations are equivalent to “species,” but this represents an exciting and refreshingly novel approach to letting genome sequences tell us what we should be paying attention to.

Jessica and I enjoyed writing Perspective for new Science paper on evolvability

None of us are looking for extra work to do, but when invited to write a Perspective for this great paper out of the lab of Andreas Wagner, Jessica Lee (now at Global Viral) and I made time to make it happen. The Research Article from Zheng et al. – “Cryptic genetic variation accelerates evolution by opening access to diverse adaptive peaks” (Science, 2019. 365:347-353) – took advantage of the ability to select upon fluorescent proteins in a FACS machine to impose various selective pressures. They permitted cryptic variation to accumulate by imposing purifying selection upon yellow fluorescence for yfp variants. They then used this pool to begin selecting upon the upper range of green fluorescence. These diverse pools adapted faster and through a wider variety of paths than if they just began with the single ancestral yfp variant.

In our Perspective – “Tales from the cryp(ic)” (Science, 2019. 365:318-319) – we enjoyed pointing out comparisons to some awesome work of friends and colleagues that touched upon these questions: Jeremey Draghi‘s exploration of robustness, Eric Hayden‘s similar work with ribozymes, and Joe Thornton and Mike Harm‘s use of ancestral reconstruction to look at epistasis from a historical perspective.

Great commentary by Jennifer Farrell and Sam Brown on our new PNAS paper

Screen Shot 2018-11-28 at 12.55.42 PMWhat a wonderful surprise! I had no idea PNAS was doing a commentary on our paper, and then I found this excellent piece written by Jennifer Farrell and Sam Brown (Georgia Tech). They end their piece hoping that Will Harcombe (now at U. Minnesota) continued to evolve the two-species system described in this paper. Thankfully I know the answer is yes, and there will be more good stuff to come that he has carried forward in his own lab.

Review published on role of sequencing in revolutionizing studies of experimental evolution.

Screen Shot 2018-11-16 at 5.43.20 PMEric Bruger and I penned a review (Bruger and Marx, 2018. Current Opinion in Microbiology) that seeks to address the manner in which sequencing technologies have opened the door to whole new questions in experimental evolution. It was a joy to highlight the incredible work our field has accomplished in such a short time. I knew sequencing would be coming when I started my lab in 2005, but the magnitude of change has been incredible.

Two papers led by Will Harcombe – one in PNAS – on cooperation in synthetic communities

In the past months we have had two papers on the E. coliS. enterica system that Will Harcombe developed, and worked on when he was a postdoc in the lab.

One of these (Hynes et al., 2018. Biomedical Physics and Engineering Express) reports the ability to examine communities via bioprinting, and also represented a collaboration with two of my best friends Daniel Segrè and Nate Cady.

The second of these (Harcombe et al., 2018. PNAS) just came out a few weeks ago online in PNAS. It describes Will’s amazing finding of bidirectional costly mutualism evolving between species in the lab. Repeatedly E. coli evolved to break its own metabolism to excrete galactose to S. enterica during growth together on lactose (which S. enterica can’t use) in order to obtain methionine, which S. enterica had previously evolved to produce in return. I was excited to discover that, just a couple days ago, PNAS published a commentary on our paper penned by Jennifer Farrell and Sam Brown.

Papers stemming from KnipBio

Screen Shot 2018-11-16 at 5.13.21 PMBack in 2013, I co-founded KnipBio with Larry Feinberg. KnipBio’s goal is to develop Methylobacterium as an aquaculture feed ingredient that can simultaneously reduce the need for fishmeal-derived protein and provide high-value components and properties. In the past two years, our first publications have come out describing the successful use of this single-cell protein with a variety of aquaculture species (Tlusty et al., 2017. PeerJ, Hardy et al., 2018. Aquaculture Research). It has been very exciting to see work move from the lab and translate to practical outcomes.

Congrats to Siavash for a successful PhD defense

IMG_3898This past Tuesday, 11/13, Siavash Riazi presented his defense for a PhD in BCB entitled “Mathematical modeling and analysis of gene expression to understand phenotypic heterogeneity and the response of Methylobacterium extorquens to formaldehyde toxicity.” His work was co-advised by Chris Remien (Mathematics) and me, and represents his first PhD student, and my first to finish here at Idaho. Many thanks to committee members, Holly Wichman, Steve Krone, and Craig Miller. And most of all congrats to Dr. Riazi!