Download Master Microbiology Evolution of the Eukaryotic Cell

Master Microbiology
Evolution of the Eukaryotic Cell
LITERATURE
Dagan T, Martin W (2004)
The tree of one percent.
Genome Biology 7: 118
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
Prof. Dr. Ralf Rabus
AG Allgemeine und Molekulare Mikrobiologie
Institut für Chemie und Biologie des Meeres (ICBM)
© Ralf Rabus, www.icbm.de
Contents
Prokaryotes versus Eukaryotes
Tree of life?
Five current views of microbial evolution
Archezoa - early-branching eukaryotic lineages?
Mitochondria in multiple guises
Models of eukaryote origin
Timing and ecological context of eukaryote origins
Genetic control of biogenesis of mitochondria and chloroplasts
Genome reduction in mitochondria and plastides
© Ralf Rabus, www.icbm.de
Prokaryotes versus Eukaryotes
Bacterial cell
Animal cell
Plant cell
Cell wall
Plasmamembrane
Plasmamembrane
Cell wall
Plasmamembrane
Ribosome
Polysome
Cytoplasm
Chromosome
Plasmid
Ribosome
Polysome
Cytoplasm
Mitochondrium
Goli apparatus
ER
Nuclear membrane
Nucleus
Nucleolus
Ribosome
Polysome
Cytoplasm
Mitochondrium
Goli apparatus
ER
Nuclear membrane
Nucleus
Nucleolus
Pore
Chlorplast
Vacuole
© Ralf Rabus, www.icbm.de
Fuchs
Allg. Mirko.
(2006) Abb. 2.2
Tree of life: the bifurcation dilemma
Classical view of evolution: phylogeny as a tree-like process of lineage splitting
tree of life = single bifurcating tree
lateral gene transfer (LGT) no major impact on evolution
microbial genomes are related by a series of bifurcations
LGT is important among prokaryotes
proportion of prokaryotic genes affected by LGT: 2-60%
LGT occurred throughout microbial history
LGT is not tree-like
microbial evolution undepictable by a single bifurcating tree
Endosymbiotic gene transfer (among eukaryotes) adds to the bifurcation dilemma
mitochondria originate from an ancestral D-proteobacterium
chloroplasts originate from an ancestral cyanobacterium
© Ralf Rabus, www.icbm.de
Dagan
Allg. &
Mirko.
Martin (2006)
Tree of life: genomic perspective (I)
Automatable procedure for reconstructing the tree of life
identify protein families that are universally distributed among all genomes
detect cases of LGT (unusual tree topologies)
exclude such proteins and reiterate the procedure
31 presumably orthologous proteins sequences present in 191 genomes each
31 proteins represent about 1% / 0.1% of an average prokaryotic / eukaryotic proteome
tree of 1% or 0.1%
exclusion of all non-universally distributed proteins and suspected cases of LGT
Support a Gram-positive origin of Bacteria and suggest a thermophilic last universal
common ancestor
© Ralf Rabus, www.icbm.de
Ciccarelli et al. (2006)
Tree of life: the genomic perspective (II)
Archaea
Eukaryota
Bacteria
© Ralf Rabus, www.icbm.de
Ciccarelli et al. (2006) Fig. 2
Tree of life: the genomic perspective (III)
non-redundant set of human proteins against all proteins from 224 prokaryotic genomes
200 eubacteria
31 universal proteins for tree of life
no. of proteins
% amino-acid identity
24 archaebacteria
© Ralf Rabus, www.icbm.de
Dagan & Martin (2006) Fig. 2
Five current views of microbial evolution
The classical rRNA-derived tree
The introns-early tree
The neomuran tree
The symbiotic tree
The prokaryote-host tree
© Ralf Rabus, www.icbm.de
Dagan & Martin (2006)
The classical rRNA-derived tree
The universal ancestor (progenote):
communal collection of information-storing and processing entities
not yet organized as cells
LGT main mode of genetic novelty
"Genetic annealing" gives rise to cells:
order of domain branching off: Eubacteria, Archaebacteria and then Eukaryotes
refractory to LGT and endosymbiotic GT negligible for evolution
© Ralf Rabus, www.icbm.de
Dagan & Martin (2006) Fig. 1a
The introns-early (or eukaryotes-first) tree
The ancestral state of genes might be "split"
some introns in eukaryotes = carryovers from the assembly of primordial
protein-encoding regions
organization of eukaryotic genes (having introns) represents that of the first genome
intronless prokaryotes would be a derived conditions
© Ralf Rabus, www.icbm.de
Dagan & Martin (2006) Fig. 1b
The neomuran tree
The common ancestor: free-living eubacterium (Chlorobium-like anoxygenic phototroph)
Eubacteria only organisms on Earth until 900 Mio. years ago
At this time an Actinobacterium-like eubacterium lost its murein-containing cell wall
reinvention of the cell wall by a group of rapidly evolving organisms (Neomura)
invention of isoprene ether lipid synthesis Æ archaebacteria
phagotrophy Æ eukaryotes
Accounts for cell biological characters, but not for sequence similarities among genes
© Ralf Rabus, www.icbm.de
Dagan & Martin (2006) Fig. 1c
The symbiotic tree: a merger of distinct branches
Ancestor of eukaryotes: endosymbiosis of prokaryote X in host prokaryote Y
formation of nucleated (n) cells
Subsequent separate endosymbiotic events between eukaryotic host and prokaryotes:
ancestor of plastides (p) and mitochondria (m)
© Ralf Rabus, www.icbm.de
Dagan & Martin (2006) Fig. 1d
The prokaryote-tree with LGT: a merger of ephemeral genomes
Extensive LGT throughout microbial evolution (inset 1)
No mitochondria-lacking eukaryotes observed so far
Endosymbiotic origin of plastids and mitochondria (endosymbiotic event in a prokaryote!)
ring-like relationship (inset 2) between ancestral organisms rather than a tree
© Ralf Rabus, www.icbm.de
Dagan & Martin (2006) Fig. 1e
Where to go?
Recover and depict both, the tree-like and non-tree-like mechanisms of microbial evolution
tree-like: vertical inheritance through common descent
non-tree-like: LGT and endosymbiosis
© Ralf Rabus, www.icbm.de
Dagan & Martin (2006)
Archezoa - early-branching eukaryotic lineages?
Archezoa
mostly anaerobic or parasitic eukaryotes
once thought to lack mitochondria
first: divergence of Archezoa; second: mitochondrial aquisition
© Ralf Rabus, www.icbm.de
Embley & Martin (2006) Fig. 1
Mitochondria in multiple guises
Archezoa are now known to contain mitochondria-related organelles
hydrogenosomes and mitosomes (also in ciliates and fungi, not grouped with Archezoa)
common trait: double membrane and conserved mechanisms of protein import
share at least one further trait with mitochondria
Absence of traditional mitochondria and presence of a specialized anaerobic phenotype
are neither rare nor "primitive" as once thought
Aerobic and anaerobic eukaryotes, harbouring mitochondrial homologues of various
sorts, have co-existed throughout eukaryote history
© Ralf Rabus, www.icbm.de
Embley & Martin (2006)
Mitochondria
Possess a genome encoding components
involved in oxidative phosphorylation
Transport of ATP into cytosol
Key enzymes of anaerobic metabolism
(e.g. pyruvate:ferredoxin oxidoreductase)
in anaerobically functioning mitochondria
(e.g. protists like Euglena)
© Ralf Rabus, www.icbm.de
Embley & Martin (2006) Fig. 2a
Hydrogenosomes
No genome
Oxidation of pyruvate to H2, CO2 and acetate
Key enzymes of anaerobic metabolism
(e.g. pyruvate:ferredoxin oxidoreductase)
ATP-generation via substrate-level phosphorylation
Transport of ATP into cytosol
Single common ancestry of mitochondria and
hydrogenosomes very likely
© Ralf Rabus, www.icbm.de
Embley & Martin (2006) Fig. 2b
Mitosomes
No genome
Undergone more evolutionary reduction than
hydrogenosomes
No direct role in ATP synthesis
In Giardia: two mitochondrial proteins of Fe/S cluster
assembly
Occurrence in:
eukaryotes with cytosolic ATP synthesis
energy parasites
© Ralf Rabus, www.icbm.de
Embley & Martin (2006) Fig. 2b
Models of eukaryote origin
1. Nucleus bearing, amitochondriate cells
2. Acquisition of mitochondria in an eukaryotic host
© Ralf Rabus, www.icbm.de
1. Origin of mitochondria in a prokaryotic host
2. Acquistion of eukaryote-specific features
Embley & Martin (2006) Fig. 4
Timing and ecological context of eukaryote origins: classical view
Diversified unicellular microfossils (widely accepted as eukaryotes) appear in strata
of ~1.45 billion years (Gyr)
Minimum age of eukaryotes at ~1.45 Gyr
Fossilized Bangiomorpha (strongly resembling modern bangiophyte red algae) appear
in strata of ~1.2 billion years (Gyr)
Minimum age of plant kingdom at ~1.2 Gyr
Two main stages in early eukaryotic evolution
early emergence and diversification of anaerobic, amitochondriate lineages
acquisition of an oxygen-respiring mitochondrial ancestor in one lineage Æ diversification
of aerobic eukaryotic lineages
global rise in atmospheric oxygen levels at ~2 Gyr ago Æ "environmental disaster"
for cells lacking the mitochondrial endosymbiont
© Ralf Rabus, www.icbm.de
Embley & Martin (2006)
Timing and ecological context of eukaryote origins: critical view
Contemporary anaerobic eukaryotes did not branch off before the origin of mitochondria
New isotopic studies indicate that anaerobic environments persisted locally and globally
over the past 2 Gyr
oxygen appeared first in the atmosphere at ~ 2 Gyr ago
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 from
anoxic 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
Embley & Martin (2006)
Genetic control of biogenesis of mitochondria and chloroplasts
c Massive transfer of ancestor derived genes into the nucleus
Æ only few genes retained in the genomes of the organelle
d Organelles strongly depend on nuclear genes Æ 90% of proteins imported from cytosol
e DNA still transferred from organelles to nulceus
c
e
d
e
c
© Ralf Rabus, www.icbm.de
Timmis et al. (2006) Fig. 1
Genome reduction in mitochondria and plastides
Sequenced mitochondrial genomes encode 3 - 67 proteins
modern D-proteobacterium Mesorhizobium loti: 7 Mb genome encodes >6,700 proteins
Sequenced plastide genomes encode 20 - 200 proteins
cyanobacterium Nostoc punctiforme: >9 Mb genome encodes >7,200 proteins
enormous reduction of organelle genome
Genome reduction in organelles versus parasites
parasites: reduction through specialisation to a nutrient-rich intracellular environment
Æ loss of genes that are no longer needed
organelles: reduction through export of essential genes to the host´s genetic apparatus
Æ import of thousands of essential proteins from the cytosol
© Ralf Rabus, www.icbm.de
Reduction of chloroplast genome
Time course of gene relocation
massively at the onset of endosymbiosis
continued during lineage diversification
The same core set of genes (photosynthesis
and translation) retained in all lineages
Displayed lineage diversification
red algae (Porphyra)
angiosperms (flowering plants)
Cyanophora (belonging to the most ancient
lineage of photosynthetic eukaryotes)
© Ralf Rabus, www.icbm.de
Timmis et al. (2006) Fig. 2
Acquisition of plant-like genes in trypanosomes
Martin and Borst (2003) PNAS 100:765-767