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Conference abstracts from the Colloqium
Microbial Evolution: Concepts and Controversies
organised by
The Canada Research Chair in the history of biology
at the
Université du Québec à Montréal, from October 17 to 19 2002
Beyond neo-Darwinism: The Origins of Microbial Phylogenetics
Jan Sapp
Department fo History, Université du Québec à Montréal, CIRST
Chairholder of the Canada Research Chair in the History of Biology
The neo-Darwinian evolutionary synthesis of the 1930s and 1940s dealt with the evolution of
plants and animals over the last 560 million years. It did not address the evolution of
microorganisms and the previous 3000 million years of evolutionary change on earth. During the
last two decades of the twentieth century, biologists developed new comparative molecular
techniques and concepts to trace life back thousands of millions of years to investigate early
microbial evolution with the aim to create a universal phylogeny. Studies of microbial phylogeny
have brought about a conceptual revolution in the way in which evolutionary change occurs in
microbes with the evidence for the fundamental importance of symbiotic mergers, fusions, and
various other mechanisms for horizontal gene transfer. The scope and significance of these
mechanisms remain subjects of controversy.
The Origin of Intermediate Metabolism
Harold Morowitz
Krasnow Institute, George Mason University, Fairfax, VA 2030, USA
The case is made for autotrophs preceding heterotrophs, chemoautorophs preceding
photoautotrophs, and the reductive tricarboxylic acid cycle preceding the Calvin-Benson cycle.
The acetyl Co-A pathway is less certain. A group of universal features of the primary chart of
autotrophic metabolism is discussed. This includes the universal nitrogen entry point and the
universal sulfur entry point. The ecological significance of universal features of primary
metabolism is discussed. The existence of biological laws at various hierarchical levels is
outlined. The Pauli Exclusion Principle is presented as an example of hierarchical laws. The
anomalous features of Vitamin B12 are discussed.
Molecular phylogeny of bacteria based on comparative sequence analysis of conserved
genes
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Karl Heinz Schleifer and Wolfgang Ludwig
Department of Microbiology, Technical University Munich, Am Hochanger 4, D-85350 Freising; Germany
Carl Woese and his coworkers achieved a breakthrough regarding the reconstruction of the
phylogeny of prokaryotes by introducing rapid methods for comparative sequence analysis of
small subunit rRNAs. Based on their data a phylogenetic tree of prokaryotes could be
reconstructed for the first time. Currently more than 30000 small subunit rRNA sequences from
pro- and eukaryotes are available in public databases. Due to the lack of comprehensive
sequence data bases for other potential phylogenetic marker molecules, our view of the
phylogeny of bacteria is mainly based on data derived from only one class of molecule, the
16S rRNA. Now in the era of genomics the rapidly increasing number of accessible full
genome and further gene sequence data allows a sound evaluation of small subunit rRNA
based phylogenetic conclusions. The comparative analysis of the available genome data showed
that only a rather limited number of genes or gene products fulfils the criteria for phylogentic
markers such as universal distribution as well as sufficient sequence conservation and
complexity. The large subunit rRNA, elongation and initiation factors, subunits of proton
translocation ATPase, RNA polymerase, DNA gyrase, recA, heat shock proteins, and amino
acyl tRNA synthetases are among the most informative marker molecules. Comparative
phylogenetic analyses of these markers are in good agreement with that of the small subunit
rRNA, at least with respect to the major groups. However, local tree topologies often differ
depending on the molecule analysed. This was to be expected. In a few cases there are also
more drastic differences between phylogenetic trees derived from rRNA and protein genes.
This, however, can mostly be explained by the presence of multiple genes which may originate
from gene duplication or lateral gene transfer. Since functional consistency of multiple genes
cannot be assumed for all variants, there may be the risk of comparing paralogous markers.
The latter can only be recognized as such if there are genomes containing all variants of the
multiple genes. This may complicate comparative phylogenetic analysis. However, with the
availability of more full genome sequences it should be possible to handle such problems more
properly.Despite the problems with multiple genes, the phylogenetic analyses based upon
different alternative markers showed that small subunit rRNA derived trees globally reflect the
phylogeny of the corresponding organisms, however, locally more their own history.
Interactions between Horizontal Gene Transfer and the Environment.
James Lake and R. Jain, M. Rivera, J. Moore
Molecular Biology Institure, University of California, Los Angeles
Horizontal gene transfer (HGT) is a process through which disparate prokaryotic groups can
obtain foreign genetic material in response to a changing environment. It is an ancient process
that has altered genomes since, at least, the last common ancestor of life and is influenced by
abiotic factors such as temperature and pH. HGT is selective and preferentially favors the
exchange of some gene types. Operational genes (mostly housekeeping genes) are readily
incorporated through HGT, but informational genes (translation, transcription, and other genes)
are less readily incorporated through this mechanism. HGT is also influenced by abiotic factors
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such as temperature and pH. It has been suggested that the collection of organisms that
exchange genes can be thought of as a globalorganism, having an immense population size and a
correspondingly great potential for evolving novel genes. Here we ask whether the organisms
which share genes truly share them on a global scale, or whether environmental factors can
affect its scale. In other words, can geography and environment, or abiotic and biotic
parameters, influence genetic exchange by HGT? Our analyses of some 20,000 genes in eight
complete genomes show that environmental factors can significantly alter horizontal transfer
among prokaryotes.
Mountains and molehills what is at stake in the lateral gene transfer debate?
W. Ford Doolittle
Program in Evolutionary Biology, Canadian Institute for Advanced Research and Department of Biochemistry and
Molecular Biology , Dalhousie University
During the 1980s and 90s, microbiologists constructed, and came to believe in, a universal
species tree based on sequences of a single gene (small subunit rRNA) even though they had
known since the mid 1960s that some genes can be readily transferred between species. There
were sound and unsound reasons for being optimistic about this enterprise, and many still
endorse it, although complete prokaryotic genome sequences, ever more numerous and
accessible, show that we had drastically underestimated the extent of transfer, over short and
long evolutionary time scales. I will survey the current state of this debate over gene transfer
the evidence, the arguments and the underlying reasons for the heat.
CONTEMPORARY ISSUES IN MITOCHONDRIAL ORIGINS AND EVOLUTION
Michael W. Gray
Program in Evolutionary Biology, Canadian Institute for Advanced Research and Department of Biochemistry and
Molecular Biology, Dalhousie University, Halifax, NS B3H 4H7
Questions about the origin of the mitochondrion and its subsequent evolution are intimately tied
to the mitochondrial genome, for it is the latter that has provided the clearest indications of a
bacterial (specifically a-Proteobacterial) origin for at least those functions (coupled oxidative
phosphorylation, protein synthesis) that this genome partly encodes. One of the most
remarkable features of the mitochondrial genome is its extreme structural and organizational
diversity, which underpins a basically uniform genetic function. Mitochondrial DNAs (mtDNAs)
in animals, plants, fungi and protists look very different from one another, and they evolve in
radically different ways. Comparative sequence analysis, based on the determination of
complete mtDNA sequences, has proven to be a powerful method for assessing the pathways
and processes of mitochondrial genome evolution, and for making inferences about the origin of
the mitochondrion. This approach has defined three general organizational patterns (designated
ancestral, expanded ancestral and derived) into which mitochondrial genomes can be roughly
classified, and has also identified the most gene-rich and eubacteria-like mitochondrial genomes
yet known, providing our clearest picture to date of the ancestral mtDNA progenitor. Various
types of data, including mitochondrial gene content, gene order and phylogenetic trees based on
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concatenated mitochondrial protein-coding sequences, argue strongly in favour of a single origin
of the mitochondrial genome.
Although the mitochondrial genome is essential to the process of mitochondrial
biogenesis, it encodes a relatively small number of the protein components of the mitochondrion:
genes for the vast majority of mitochondrial proteins are carried by the nuclear genome. The
availability of complete nuclear genome sequences (e.g., yeast) has provided an opportunity to
assess the phylogenetic affiliations of nucleus-encoded mitochondrial proteins. A small
proportion of these proteins can be traced unambiguously to the a-Proteobacterial lineage of
eubacteria; genes for these proteins likely resided originally in the proto-mitochondrial genome
but were transferred to the nucleus in the course of evolution. A large proportion of nucleusencoded mitochondrial proteins appear to be unique within the eukaryotic lineage, suggesting
that at least some of these proteins may have emerged specifically within this lineage. A stillcontentious question is whether any extant amitochondriate eukaryotes derive from ancestors
that primitively lacked mitochondria, or whether the amitochondriate condition is in all cases a
derived trait, due to secondary loss of the organelle in a primitive ancestor. The finding in some
amitochondriate eukaryotes of nuclear genes encoding typically “mitochondrial” proteins has
strengthened the case for secondary loss of mitochondria. Nevertheless, at this time we cannot
confidently discount the existence of primitively amitochondriate eukaryotes.
On the Origins of Cells -- Prokaryotic and Eukaryotic
William Martin
Institut für Botanik, Universität Düsseldorf, D-40225 Düsseldorf, Germany
Tel ++49-211-811-3011; Fax ++49-211-811-3554
e-mail [email protected]
The discrepancy between the number of genes that organelle genomes encode (<100) and the
number of eubacterial proteins that they contain (>1000) is generally explained by something
known as 'endosymbiotic gene transfer'- during evolution, organelles export their genes to the
nucleus, but re-import the gene products, so that proteins are retained in organelles, but most of
the genes are not. Traditional views posit that the host of mitochondrial symbiosis was a
heterotrophic, primitively amitochondriate eukaryote. The hydrogen hypothesis posits that the
heterotrophic lifestyle ancestral to all eukaryotes is an acquisition via gene transfer from a
facultatively anaerobic, heterotrophic purple non-sulphur eubacterium - the common ancestor of
mitochondria and hydrogenosomes - that became an endosymbiont in an H2-dependent,
autotrophic host. The hydrogen hypothesis provides a simple rationale to explain the findings of
i) common ancestry of mitochondria and hydrogenosomes, ii) that all eukaryotes studied to date
possessed a mitochondrial symbiont in their evolutionary past, and iii) that eukaryotes, generally
speaking, possess an archaebacterial genetic apparatus that proliferates with the help of
eubacterial energy metabolism. If time permits, some thought will be given to the origins of cells
in general.
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Evolutionary Relationships Among Prokaryotes and the Origin of the Eukaryotic Cell
Radhey S. Gupta
Department of Biochemistry, McMaster University, Hamilton, Canada L8N 3Z5
To understand the origin of the eukaryotic cell, it is essential at first to clarify the evolutionary
relationships among prokaryotic organisms which predated the eukaryotes. Our work
employing conserved inserts and deletions (indels or signature sequences) in highly conserved
proteins as phylogenetic tools is providing valuable information in this regard. Based on the
identified signatures, it is now possible to define in clear molecular terms all the main groups
within Bacteria and logically deduce how they are related to each other and in what order have
they branched off from a common ancestor. These issues, which are central to understanding
bacterial phylogeny, were not resolved in the past. The branching order of different groups is
indicated as follows: Low G+C gram-positive Y High G+C gram-positive Y ClostridiumFusobacteria- Thermotoga Y Deinococcus-Thermus- Green nonsulfur bacteria Y
Cyanobacteria Y Spirochetes Y Chlamydia-Cytophaga -Bacteroides- Green sulfur bacteria
Y Aquifex
Y Proteobacteria-1 (, and *) Y
Proteobacteria-2 (") Y
Proteobacteria-3 ($) and Y Proteobacteria -4 ((). The reliability and predictive power
of this model was objectively tested using sequence data for bacterial genomes. The model
correctly predicted the presence or absence of various indels in all 67 bacterial genomes with
only a single exception in 1322 observations (>99.9 % reliability). These results also provide
strong evidence that the genes/proteins containing these indels have not been affected by factors
such as lateral gene transfer, although such events play an important role in evolution.
Signature sequences and phylogenetic analysis based on many proteins also point to a specific
relationship between Archaebacteria and Gram-positive bacteria, a relationship which is
supported by the similarity in their cell structures. The genes/proteins which indicate Archaea to
be distinct from Bacteria are primarily those involved in the information transfer processes, and
they provide the main targets for antibiotics produced by Gram-positive bacteria. We have
suggested that both Archaebacteria and Diderm bacteria have evolved from Gram-positive
bacteria as different strategies to cope with the antibiotic selection pressure.
Unlike the evolutionary relationships among prokaryotes, the eukaryotic cells are indicated to be
of chimeric origin having received major gene contributions from both archaebacteria and
Gram-negative bacteria ("-proteobacteria). We have suggested that the formation of the
ancestral eukaryotic cell involved a unique fusion event between these two groups of
prokaryotes, which resulted in the formation of nucleus as well as ER. Our analyses also
indicate that this primary fusion event was distinct from the latter endosymbiotic event that gave
rise to mitochondria.
The missing piece: the microtubule cytoskeleton and the origin of eukaryotes
Michael F. Dolan
Department of Geosciences, University of Massachusetts, Amherst
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Eukaryotes are characterized by a membrane-bounded nucleus and a microtubule cytoskeleton
that is used to separate the chromosomes in mitosis. The recent, molecular- and biochemicalbased hypotheses on the origin of eukaryotes fail to adequately address the evolutionary origin
of microtubules. This stems in part from the replacement of morphological- and organismbased approaches to cell evolution with molecular- and biochemical-based ones.
Morphological, natural historical approaches stress the biology of contemporary organisms.
Such an approach looks for tubules or tubule-organizing centers in bacteria, or for simplified
microtubule structures in protists, and then considers the biochemical components involved.
Proponents of such approaches usually insist that the clues to the earliest lineages can be found
among extant taxa. Molecular and biochemical approaches emphasize gene or amino acid
sequences and protein chemistry, and consider the organismic biology secondarily, as in the
case of FtsZ, the putative prokaryotic tubulin homolog. Proponents of these approaches are
willing to write-off higher-level taxa, such as the primordial Eukarya or pre-mitochondrial
eukaryotes, or the pre-microtubule-containing eukaryotes, that are purported to be evolutionary
intermediates, but have left no descendants. An hypothesis on the origin of microtubules that
synthesizes both approaches is lacking.
"Thiodendron"-like consortia to chimeric archaeprotists”
Lynn Margulis
Department of Geosciences, University of Massachussetts, Amherst
Since all nucleated cells (eukaryotes) evolved via symbiogenesis from at least two kinds of
ancestors (as did no bacterial cells, prokaryotes), the three domain classification system
(Archeae, Bacteria, Eukarya) is inadequate and misleading. To those who seek logical,
descriptive and useful classification systems all living organisms can be placed unambiguoulsy
into one or another of the two highest taxa (most inclusive groups): Prokaryotae and
Eukaryotae. All members of the four mutually exclusive unambiguous taxa of eukaryotes, by
hypothesis, evolved from anaerobic prokaryotic consortia similar to the extant Thiodendron
association. From an analogous prokaryotic consortium of a sulfur-reducing archaebacterium
(like Thermoplasma acidophila) and a motile sulfide-oxidizing eubacterium (like the
Spirochaeta of Thiodendron) evolved the chimeric ancestor (such as that suggested by
Gupta). The descendants of the chimera include mitotic anaerobes (archaeprotists) such as the
amitochondriate amoebae, the diplomonads and the parabasalids The former attachment
apparatus of the consortium became the karyomastigont (organellar system of nucleus,
kinetosome and their connector). Karyomastigont then became mitotic spindle, the single
distinguishing aspect of all nucleated organisms. The nucleus evolved by release in several
lineages, both without and with mitochondria.
The role of symbiotic bacteria in eukaryotic speciation
John H. Werren
Biology Department, University of Rochester, Rochester, N.Y. 14627
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Symbiotic bacteria are widespread in nature and could play important roles in the rates and
patterns of speciation in their eukaryotic hosts. Here the empirical and recent theoretical
investigations of the role potential role of symbionts in eukaryotic speciation is explored.
Special attention is paid the endosymbiont Wolbachia, which is widespread in arthropods and
causes various reproductive manipulations in its hosts that may promote reproductive isolation
and speciation. However, more general principles that relate to the diverse array of
endosymbiont-host evolutionary interactions are also considered. Future direction of research
to evaluate the role of endosymbionts in eukaryotic speciaton are discussed.
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