Sexy paper just out in PLoS ONE

My lab has taken its initial journey on the PLoS ONE train.

Yesterday, our paper entitled "An Expanded Inventory of Conserved Meiotic Genes Provides Evidence for Sex in Trichomonas vaginalis" was published in PLoS ONE. It's a updated and detailed report on the ongoing work in my lab to generate and curate an "inventory" of genes involved in meiosis that are present across major eukaryotic lineages. This paper focuses on the protist, Trichomonas vaginalis, an organism not known to have a sexual phase in its life cycle.

Here is the Abstract:

Meiosis is a defining feature of eukaryotes but its phylogenetic distribution has not been broadly determined, especially among eukaryotic microorganisms (i.e. protists)—which represent the majority of eukaryotic ‘supergroups’. We surveyed genomes of animals, fungi, plants and protists for meiotic genes, focusing on the evolutionarily divergent parasitic protist Trichomonas vaginalis. We identified homologs of 29 components of the meiotic recombination machinery, as well as the synaptonemal and meiotic sister chromatid cohesion complexes. T. vaginalis has orthologs of 27 of 29 meiotic genes, including eight of nine genes that encode meiosis-specific proteins in model organisms. Although meiosis has not been observed in T. vaginalis, our findings suggest it is either currently sexual or a recent asexual, consistent with observed, albeit unusual, sexual cycles in their distant parabasalid relatives, the hypermastigotes. T. vaginalis may use meiotic gene homologs to mediate homologous recombination and genetic exchange. Overall, this expanded inventory of meiotic genes forms a useful “meiosis detection toolkit”. Our analyses indicate that these meiotic genes arose, or were already present, early in eukaryotic evolution; thus, the eukaryotic cenancestor contained most or all components of this set and was likely capable of performing meiotic recombination using near-universal meiotic machinery.

Here are my impressions of publishing in PLoS ONE (so far)...

PROS:

• It was fast. Submission to acceptance was less than a month. It took us longer to revise the final copy than to gain initial acceptance.
• The PLoS editorial staff were very accommodating and helpful throughout the process. In particular, they quickly transferred our manuscript between other PLoS journals (where it was initially rejected).
• The review process was great. In this case, only one reviewer was contacted. S/he liked the paper, and gave some suggestions for improvement that were left up to us to incorporate. We heeded some, but not all of the advice given.
  
• It was (fairly) inexpensive. The "page charges" ($1125) were ~40% less than those levied for a similar non-OA journal that we have published in recently.

CONS:

• There was no opportunity given for making corrections to proofs. I have already identified an issue with one of the tables that would have been corrected in proof had there been an opportunity. There are always a few things that the author can notice that the copy editors (however talented they are) might miss. Why not add the author as a final checker?
• The Journal Management System (for e-submission and tracking) is a bit too complicated for my taste. It takes quite a while (1+ hour) to get all of the information pasted into the form. I may just need to get to used to this level of front-end effort. However, as noted above, the journal staff helped me by moving all of the manuscript info from one journal to another. If not, it would have been painful to repeat.
  
• As of this posting, our paper has not yet appeared in the listing of papers published yesterday. I assume (and hope) that this is a small and non-frequent oversight, but an annoying one when it's my paper!

I think that the PROS much outweigh the CONS in this case. Direct any comments on the paper itself to the PLoS ONE site.

Evolution of Meiotic Genes: The Case of Spo11

In the vein of shameless self-promotion, it's my pleasure to announce that a recent paper from my lab has just been published as an Advance Access article in Molecular Biology & Evolution: Protist Homologs of the Meiotic Spo11 Gene and Topoisomerase VI Reveal an Evolutionary History of Gene Duplication and Lineage-Specific Loss (Shehre-Banoo Malik, Marilee A. Ramesh, Alissa M. Hulstrand & John M. Logsdon, Jr., Molecular Biology & Evolution, in press).

This paper is the first in a series of papers that is emerging from Banoo Malik's PhD thesis and is a result of a long-standing project with former postdoc Marilee Ramesh (now at Roanoke College). It's also the first of a number of meiotic "gene stories" that we have been untangling over the past few years. The image shown is a summary of the phylogenetic distribution of Spo11 homologs that we determined. The paper is not Open Access (sorry); however, if you are interested in reading it and do not have a subscription to MB&E, drop me an email.

Abstract
Spo11 is a meiotic protein of fundamental importance as it is a conserved meiosis-specific transesterase required for meiotic recombination initiation in fungi, animals and plants. Spo11 is homologous to the archaebacterial topoisomerase VIA (Top6A) gene, and its homologs are broadly distributed among eukaryotes, with some eukaryotes having more than one homolog. However, the evolutionary relationships among these genes are unclear, with some debate as to whether eukaryotic homologs originated by lateral gene transfer. We have identified and characterized protist Spo11 homologs by degenerate PCR and sequencing and by analyses of sequences from public databases. Our phylogenetic analyses show that Spo11 homologs evolved by two ancient eukaryotic gene duplication events prior to the last common ancestor of extant eukaryotes, resulting in three eukaryotic paralogs: Spo11-1, Spo11-2 and Spo11-3. Spo11-1 orthologs encode meiosis-specific proteins and are distributed broadly among eukaryotic lineages, though Spo11-1 is absent from some protists. This absence coincides with the presence of Spo11-2 orthologs, which are meiosis-specific in Arabidopsis and are found in plants, red algae and some protists, but absent in animals and fungi. Spo11-3 encodes a Top6A subunit that interacts with topoisomerase VIB (Top6B) subunits, which together play a role in vegetative growth in Arabidopsis. We identified Spo11-3 (Top6A) and Top6B homologs in plants, red algae, and a few protists, establishing a broader distribution of these genes among eukaryotes, indicating their likely vertical descent followed by lineage-specific loss.

Promoting Plants at the Expense of Fungi?

Ryan Gregory, over at Genomicron, found an interesting tidbit on the Discovery Channel website entitled Plants and Animals: Long-Lost Relatives?. He is surprised to read that

"organisms such as fungi should be given a demotion — placed further from animals on the tree — while green plants should get a leg up."

This is the case, apparently according to a recently-published paper from John Stiller at East Carolina University.

Gregory is (rightfully) annoyed at the suggestion of any group "getting "demoted" one way or another because this idea of rank (was) should have been abandoned 150 years ago." and that was the main point of his post. Ryan has been (again, rightfully) critical of science reporting and this doozey has all of the right parts, as detailed in his Anatomy of a bad science story.

However, there have been a series of comments about the veracity of the Stiller paper, so I thought I would make a few of my own here. First of all, it should be duly noted that the paper in question, Plastid endosymbiosis, genome evolution and the origin of green plants, is explicitly labelled as "Opinion"; this is on top of the fact that it is published in the review journal TRENDS in Plant Science—not a primary research venue. Neither of these facts are damning to the work, but they certainly suggest caution in reporting the findings.

Second, it is fair to say that this hypothesis (wrongly called "Stiller's theory" by the Discovery story) is way out of the mainstream of current thought. Again, this alone should neither preclude the publication nor, by itself, lend it to immediate scorn. It's great to see such examples of how science works in the marketplace of ideas. But we all know that just because something gets published, does not mean it's right.

In any case, there are two main components that Stiller argues in this paper:

1. that the "Plantae" [Viridiplantae (green algae & land plants), Rhodphyta (red algae) and Glaucocystophyta] are not a monophyletic group, and
2. that the Viridiplantae are more closely related to animals than are fungi.

The data on "Plantae" monophyly are certainly not so compelling as to rule out other possible answers. But recent work (here and here) is increasingly providing support for this relationship. Stiller has been a long-standing contributor to the literature on non-monophyly of green+red algae. I have worked on some of the same molecules that he has (i.e., RNA pol II) and he might have a point for there not being strong support in favor of "Plantae". However, I don't think that there is an alternative that garners anywhere near the consistent support that "Plantae" gets in multigene trees.

The data on the sisterhood of animals and fungi grouping to the exclusion of plants (e.g., Viridiplantae) is about as solid as deep relationships among eukaryotes can be. A nice summary of these results was recently presented in PLoS Genetics. Since the paper is Open Access, I won't repeat the findings here (full disclosure: although I am not an author of this paper, I do collaborate with them). Suffice it to say that there is not even a hint of evidence that Viridiplantae is closer to animals that are fungi as suggested by Stiller. Note also that these authors are not particularly bullish on "Plantae" either.

Stiller cites the presence of certain enzymes and protein domains in both plants and animals (apparently absent in the fungi) as evidence for a closer relationship of plants to animals. But the problem is that such things only have to be lost once in the fungal lineage (if they have been lost at all) to make these cases complete non-sequiturs. To explain why plants don't fit in with animals, Stiller would rather invoke some sort of bias in the data. Although such biases may exist, I am very cautious about invoking an entire reworking of the tree based on them.

Stiller ends with four "Future Perspectives" of which I find the following most telling:

"There should be no a priori assumption that the strongest tree-building signal in a given data set reflects evolutionary history rather than bias in the data."

I'll file that in the category of "Things that make you say Hmmm".

Sexy Fungi

I just found out that ASM Press has recently published a new book entitled "Sex in Fungi: Molecular Determination and Evolutionary Implications", (Editors: J. Heitman, J.W. Kronstad, J.W. Taylor, & L. A. Casselton; ISBN: 978-1-55581-421-2). My Department colleague, David Soll, who wrote a chapter on mating type switching in Candida, let me borrow his copy for the weekend. It looks really great.

The release of this book is good timing for me, too. I have a recently-funded project in my lab to study the evolution of sex and meiosis in diverse fungi. A postdoctoral position is available in my lab immediately to work on this project. Send me an email if you are interested in hearing more.

Why Rosie doesn't work on Sex

My friend and colleague, Rosie Redfield, has written an interesting post about the origin of eukaryotic sex, entitled "Why I don't work on sex in eukaryotes ". She sums up what we do and don't know about deep eukaryotic relationships and how this impinges on the origin of sex and meiosis. One bottom line is that we still don't know what the earliest branch on the eukaryotic tree is. The other is that it might not matter for the origin of meiosis since work in my lab has shown that homologs of meiotic genes are present in all of the major protist lineages (e.g, this paper, but stay tuned for more details...). Rosie ends her provocative post by paying me a sincere compliment:

"I'm glad that John Logsdon has been working on this, rather than me."

Thanks, Rosie!

Shehre-Banoo Malik, PhD!

Hearty congratulations are well in order for Banoo Malik, who successfully defended her PhD thesis last Thursday (June 14th). Banoo is the first student in my lab to both start and finish a PhD under my supervision. In her case, that entailed moving with my lab from Emory University to the University of Iowa. She has been a major player in my lab group and her work has made considerable, long-lasting impacts on the lab's research.

Banoo's dissertation, entitled "The early evolution of meiotic genes", is based on her in-depth analyses of the evolutionary histories of meiotic genes. She gave a really terrific talk on her work that led to a extensive series of questions from the audience. Banoo then successfully held court with her committee, who spent some of the time arguing amongst themselves on matters of scientific import (always a good thing in a defense!). The meeting was immediately followed by a celebration including bubbly liquid. On the following day, a party in her honor was held at my home. Good job, Banoo!

Banning the word "prokaryote"

Here I am at the the American Society for Microbiology annual meeting which is being held in Toronto. As Larry Moran has already pointed out, there are a few of us bloggers that are getting together with him while we are here. This should be great.

My first day (actually, part day) was capped off with a really fun, but in many ways maddening, lecture from Norman Pace. Norm was on my PhD committee, and it was the first time I had seen him for 12 years. The talk was wonderfully vintage Norm—even some of the phrases were the same as I remembered. That's not to say that the talk was at all tired. Norm is so fun to see in the spotlight; in this case, he had a big and well-deserved stage on which to perform! As an historical aside, Norm's class on the biochemistry of nucleic acids at Indiana University was the only biochemistry course that I ever took that started by reference to a rRNA tree of life. Norm has been ahead of the curve for a long time...

A major—and provocative—theme of Norm's talk is that we microbiologists should strike the word "procaryote" (or prokaryote, as I prefer to spell it) from our vocabulary. This is not a trivial matter for the microbiologists in attendance, both from practical and intellectual points of view. This part of his talk followed directly from his recently published piece in Nature entitled "Time for a change." (2006) 441:289. I happen to strongly disagree with Norm on this point and am much more aligned with the views subsequently published by Martin & Koonin entitled "A positive definition of prokaryotes" in Nature (2006) 442: 868. Although I'm too short on energy to do so now, I'll try to decipher my notes and give a more clear account of what Norm said (and my reactions to it) in the coming days.

Evolution of Eukaryotes—Early or Late?

It was inevitable. In this week's Science magazine there is a Letter by Martin, Dagan, Koonin, Dipippo, Gogarten and Lake. They forcefully deconstruct a paper, "Genomics and the Irreducible Nature of Eukaryote Cell" that Kurland, Collins and Penny published last year in Science. There was some popular press that followed the original publication.

The Kurland et al. article did not—by far—represent the consensus view of scientists working on eukaryotic origins. However, this paper has, until now, gone without much challenge in the literature (although it shows 11 citations at ISI).

Kurland et al. argued for the (early) emergence of eukaryotes prior to prokaryotes:

"...we favor the idea that the host that acquired the mitochondrial endosymbiont was a unicellular eukaryote predator, a raptor. The emergence of unicellular raptors would have had a major ecological impact on the evolution of the gentler descendants of the common ancestor. These may have responded with several adaptive strategies: They might outproduce the raptors by rapid growth or hide from raptors by adapting to extreme environments. Thus, the hypothetical eukaryote raptors may have driven the evolution of their autotrophic, heterotrophic, and saprotrophic cousins in a reductive mode that put a premium on the relatively fast-growing, streamlined cell types we call prokaryotes."

In essence, complex eukaryotes came first, followed by prokaryotes which evolved by reduction. In today's letter, Martin et al. point out that this is a re-clothed view of eukaryotic evolution that was popular in the early 1980s. At the time, this idea was mostly centered on the origin and evolution of introns, which were assumed by some to be responsible for building the ancestral set of protein-coding genes by exon shuffling (the introns-early view); to be true, massive intron loss must have characterized the (reductive) evolution of prokaryotes. This scenario has since been thoroughly debunked. Although Kurland et al.'s hypothesis includes more than introns, it suffers from the same problems that led to the demise of introns-early.

In their response, Kurland, Collins and Penny insist that:

"...cellular and molecular biology, especially genomics, reveals signs of an ancient complexity of the eukaryotic cell. This new information was not available to older hypotheses for eukaryote origins..."

I don't find Kurland et al.'s arguments any more compelling than when I first encountered them almost twenty years ago. However, it's great to see these important questions being discussed on the pages on Science.

Picture and caption from MSNBC (Lesley Joan Collins/Science).
"This illustration shows a single-celled predator (colored brown), swallowing up much smaller and less complex single-celled bacteria (yellow and green). Researchers say such a predatory eukaryote, nicknamed "Fred the Raptor," would have had "a major ecological impact" during the early stages of cellular evolution."

The Origins of Genome Architecture

I was really excited to find in my mail yesterday a copy of Michael Lynch's new book, The Origins of Genome Architecture, just-published by Sinauer. This book represents a synthetic detailing of Mike's ideas about evolutionary principles that underlie the origin and diversification of genomes. It is very likely to become a classic in evolutionary biology. Last year, Mike published a seminal paper entitled The origins of eukaryotic gene structure in Molecular Biology & Evolution that is a precis of sorts on this topic. I am generally a big fan of his ideas, although they are not without detractors.

In full-disclosure mode, I should point out that I provided some comments to Mike on one of the chapters, resulting in the complementary book (thanks, Mike & Sinauer!). However, I have not yet had the opportunity to consider the whole book. I'll need to add it to my ever-lengthening list!

What will go here?

I probably should have thought about this some more before jumping into the deep end, but here's some of what you might find me blogging about in the near future:

Origin and Evolution of Sex. When did meiosis evolve and from what processes did it derive? Is DNA repair the original function of meiotic recombination? Are there any bona fide ancient asexual eukaryotes? If so, how do they persist?

Early Eukaryotic Evolution. What are the evolutionary relationships among the major lineages of eukaryotes? (& what are the major lineages of eukaryotes?) Can the answers provide some hints about the origin of novel features in eukaryotic cells?

Introns. What is the evolutionary history of eukaryotic gene structure? Have spliceosomal introns been mostly gained or lost during eukaryotic evolution? How? Why?

Evolution Teaching. What can be done to ameliorate the pitiful level of evolutionary knowledge in students (and the public) at all levels in the US? What information do parents and teachers need to communicate the fascinating science of evolutionary biology?

Other stuff relating to politics, religion (or lack thereof), parenting, lab management, professor-dom and other life-pusuits...