master microbiology evolution of the eukaryotic cell · prokaryotes versus eukaryotes fuchs (2006)...
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Master MicrobiologyEvolution of the Eukaryotic Cell
LITERATURE
Prof. Dr. Ralf RabusAG Allgemeine und Molekulare MikrobiologieInstitut für Chemie und Biologie des Meeres (ICBM)
Embley TM, Martin W (2006)Eukaryotic evolution, changes and challenges.Nature Reviews 440: 623-630
Timmis JN, Ayliffe MA, Huang CY, Martin W (2004)Endosymbiotic gene transfer: organelle genomes forge eukaryotic chromosomes.Nature Reviews Genetics 5: 123-135
Dagan T, Martin W (2004)The tree of one percent.Genome Biology 7: 118
© Ralf Rabus, www.icbm.de
Contents
Prokaryotes versus Eukaryotes
Tree of life?
Five current views of microbial evolution
Mitochondria in multiple guises
Genetic control of biogenesis of mitochondria and chloroplasts
Models of eukaryote origin
Archezoa - early-branching eukaryotic lineages?
Timing and ecological context of eukaryote origins
Genome reduction in mitochondria and plastides
© Ralf Rabus, www.icbm.de
Prokaryotes versus Eukaryotes
Allg. Mirko. Abb. 2.2Fuchs (2006) Abb. 2.2
Bacterial cellCell wall
PlasmamembraneRibosome
PolysomeCytoplasm
ChromosomePlasmid
Animal cell
PlasmamembraneRibosome
PolysomeCytoplasm
MitochondriumGoli apparatus
ERNuclear membrane
NucleusNucleolus
Plant cell
Cell wallPlasmamembrane
RibosomePolysome
CytoplasmMitochondrium
Goli apparatusER
Nuclear membraneNucleus
NucleolusPore
ChlorplastVacuole
© Ralf Rabus, www.icbm.de
Tree of life: the bifurcation dilemma
tree of life = single bifurcating treeClassical view of evolution: phylogeny as a tree-like process of lineage splitting
lateral gene transfer (LGT) no major impact on evolutionmicrobial genomes are related by a series of bifurcations
microbial evolution undepictable by a single bifurcating treeLGT is not tree-like
proportion of prokaryotic genes affected by LGT: 2-60%LGT is important among prokaryotes
LGT occurred throughout microbial history
Endosymbiotic gene transfer (among eukaryotes) adds to the bifurcation dilemma
Allg. Mirko. Dagan & Martin (2006)
mitochondria originate from an ancestral -proteobacteriumchloroplasts originate from an ancestral cyanobacterium
© Ralf Rabus, www.icbm.de
Tree of life: genomic perspective (I)
Ciccarelli et al. (2006)
identify protein families that are universally distributed among all genomesAutomatable procedure for reconstructing the tree of life
detect cases of LGT (unusual tree topologies)exclude such proteins and reiterate the procedure
31 presumably orthologous proteins sequences present in 191 genomes each
Support a Gram-positive origin of Bacteria and suggest a thermophilic last universalcommon ancestor
31 proteins represent about 1% / 0.1% of an average prokaryotic / eukaryotic proteometree of 1% or 0.1%exclusion of all non-universally distributed proteins and suspected cases of LGT
© Ralf Rabus, www.icbm.de
Tree of life: the genomic perspective (II)
Ciccarelli et al. (2006) Fig. 2
Archaea
Eukaryota
Bacteria
© Ralf Rabus, www.icbm.de
Tree of life: the genomic perspective (III)
non-redundant set of human proteins against all proteins from 224 prokaryotic genomes24 archaebacteria 200 eubacteria 31 universal proteins for tree of life
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Dagan & Martin (2006) Fig. 2© Ralf Rabus, www.icbm.de
Five current views of microbial evolution
The classical rRNA-derived tree
The introns-early tree
The neomuran tree
The prokaryote-host tree
The symbiotic tree
Dagan & Martin (2006)© Ralf Rabus, www.icbm.de
The classical rRNA-derived tree
"Genetic annealing" gives rise to cells:
communal collection of information-storing and processing entitiesThe universal ancestor (progenote):
not yet organized as cellsLGT main mode of genetic novelty
order of domain branching off: Eubacteria, Archaebacteria and then Eukaryotesrefractory to LGT and endosymbiotic GT negligible for evolution
Dagan & Martin (2006) Fig. 1a© Ralf Rabus, www.icbm.de
The introns-early (or eukaryotes-first) tree
some introns in eukaryotes = carryovers from the assembly of primordialprotein-encoding regions
The ancestral state of genes might be "split"
organization of eukaryotic genes (having introns) represents that of the first genomeintronless prokaryotes would be a derived conditions
Dagan & Martin (2006) Fig. 1b© Ralf Rabus, www.icbm.de
The neomuran tree
Eubacteria only organisms on Earth until 900 Mio. years agoThe common ancestor: free-living eubacterium (Chlorobium-like anoxygenic phototroph)
reinvention of the cell wall by a group of rapidly evolving organisms (Neomura)invention of isoprene ether lipid synthesis archaebacteria
At this time an Actinobacterium-like eubacterium lost its murein-containing cell wall
phagotrophy eukaryotesAccounts for cell biological characters, but not for sequence similarities among genes
Dagan & Martin (2006) Fig. 1c© Ralf Rabus, www.icbm.de
The symbiotic tree: a merger of distinct branches
Ancestor of eukaryotes: endosymbiosis of prokaryote X in host prokaryote Y
ancestor of plastides (p) and mitochondria (m)Subsequent separate endosymbiotic events between eukaryotic host and prokaryotes:
formation of nucleated (n) cells
Dagan & Martin (2006) Fig. 1d© Ralf Rabus, www.icbm.de
The prokaryote-tree with LGT: a merger of ephemeral genomes
No mitochondria-lacking eukaryotes observed so farExtensive LGT throughout microbial evolution (inset 1)
ring-like relationship (inset 2) between ancestral organisms rather than a treeEndosymbiotic origin of plastids and mitochondria (endosymbiotic event in a prokaryote!)
Dagan & Martin (2006) Fig. 1e© Ralf Rabus, www.icbm.de
Where to go?
Dagan & Martin (2006)
tree-like: vertical inheritance through common descentRecover and depict both, the tree-like and non-tree-like mechanisms of microbial evolution
non-tree-like: LGT and endosymbiosis
© Ralf Rabus, www.icbm.de
Archezoa - early-branching eukaryotic lineages?
mostly anaerobic or parasitic eukaryotesArchezoa
once thought to lack mitochondriafirst: divergence of Archezoa; second: mitochondrial aquisition
Embley & Martin (2006) Fig. 1© Ralf Rabus, www.icbm.de
Mitochondria in multiple guises
Embley & Martin (2006)
hydrogenosomes and mitosomes (also in ciliates and fungi, not grouped with Archezoa)Archezoa are now known to contain mitochondria-related organelles
share at least one further trait with mitochondriacommon trait: double membrane and conserved mechanisms of protein import
Absence of traditional mitochondria and presence of a specialized anaerobic phenotypeare neither rare nor "primitive" as once thought
Aerobic and anaerobic eukaryotes, harbouring mitochondrial homologues of varioussorts, have co-existed throughout eukaryote history
© Ralf Rabus, www.icbm.de
Mitochondria
Possess a genome encoding componentsinvolved in oxidative phosphorylation
Key enzymes of anaerobic metabolism(e.g. pyruvate:ferredoxin oxidoreductase)in anaerobically functioning mitochondria(e.g. protists like Euglena)
Embley & Martin (2006) Fig. 2a
Transport of ATP into cytosol
© Ralf Rabus, www.icbm.de
Hydrogenosomes
Embley & Martin (2006) Fig. 2b
No genome
Oxidation of pyruvate to H2, CO2 and acetate
Transport of ATP into cytosol
ATP-generation via substrate-level phosphorylation
Single common ancestry of mitochondria andhydrogenosomes very likely
Key enzymes of anaerobic metabolism(e.g. pyruvate:ferredoxin oxidoreductase)
© Ralf Rabus, www.icbm.de
Mitosomes
Embley & Martin (2006) Fig. 2b
No genome
Undergone more evolutionary reduction thanhydrogenosomes
In Giardia: two mitochondrial proteins of Fe/S clusterassembly
No direct role in ATP synthesis
Occurrence in:eukaryotes with cytosolic ATP synthesisenergy parasites
© Ralf Rabus, www.icbm.de
Models of eukaryote origin
Embley & Martin (2006) Fig. 4
1. Nucleus bearing, amitochondriate cells2. Acquisition of mitochondria in an eukaryotic host
1. Origin of mitochondria in a prokaryotic host2. Acquistion of eukaryote-specific features
© Ralf Rabus, www.icbm.de
Timing and ecological context of eukaryote origins: classical view
Embley & Martin (2006)
Diversified unicellular microfossils (widely accepted as eukaryotes) appear in strataof ~1.45 billion years (Gyr)
Minimum age of eukaryotes at ~1.45 Gyr
Fossilized Bangiomorpha (strongly resembling modern bangiophyte red algae) appearin strata of ~1.2 billion years (Gyr)
Minimum age of plant kingdom at ~1.2 Gyr
early emergence and diversification of anaerobic, amitochondriate lineagesTwo main stages in early eukaryotic evolution
acquisition of an oxygen-respiring mitochondrial ancestor in one lineage diversificationof aerobic eukaryotic lineages
global rise in atmospheric oxygen levels at ~2 Gyr ago "environmental disaster"for cells lacking the mitochondrial endosymbiont
© Ralf Rabus, www.icbm.de
Timing and ecological context of eukaryote origins: critical view
Embley & Martin (2006)
Contemporary anaerobic eukaryotes did not branch off before the origin of mitochondria
oxygen appeared first in the atmosphere at ~ 2 Gyr ago
New isotopic studies indicate that anaerobic environments persisted locally and globallyover the past 2 Gyr
up until ~ 600 Myr ago the ocean existed in an intermediate oxidation state• oxygenated surface water (where photosynthesis occurred)• sulfide-rich (sulfidic) and oxygen-lacking (anoxic) subsurface water
"oxygen event" in the atmosphere has to be decoupled fromanoxic marine environments:• anaerobic eukaryotes living on the margins of an oxic world• still valid today (e.g. water column of the Black Sea)
© Ralf Rabus, www.icbm.de
Genetic control of biogenesis of mitochondria and chloroplasts
Timmis et al. (2006) Fig. 1
Massive transfer of ancestor derived genes into the nucleusonly few genes retained in the genomes of the organelle
Organelles strongly depend on nuclear genes 90% of proteins imported from cytosol
DNA still transferred from organelles to nulceus
© Ralf Rabus, www.icbm.de
Genome reduction in mitochondria and plastides
modern -proteobacterium Mesorhizobium loti: 7 Mb genome encodes >6,700 proteinsSequenced mitochondrial genomes encode 3 - 67 proteins
cyanobacterium Nostoc punctiforme: >9 Mb genome encodes >7,200 proteinsSequenced plastide genomes encode 20 - 200 proteins
enormous reduction of organelle genome
parasites: reduction through specialisation to a nutrient-rich intracellular environmentloss of genes that are no longer needed
Genome reduction in organelles versus parasites
organelles: reduction through export of essential genes to the host´s genetic apparatusimport of thousands of essential proteins from the cytosol
© Ralf Rabus, www.icbm.de
Reduction of chloroplast genome
Timmis et al. (2006) Fig. 2
massively at the onset of endosymbiosisTime course of gene relocation
continued during lineage diversification
The same core set of genes (photosynthesisand translation) retained in all lineages
red algae (Porphyra)Displayed lineage diversification
Cyanophora (belonging to the most ancientlineage of photosynthetic eukaryotes)
angiosperms (flowering plants)
© Ralf Rabus, www.icbm.de
Acquisition of plant-like genes in trypanosomes
Martin and Borst (2003) PNAS 100:765-767