master microbiology evolution of the eukaryotic cell · prokaryotes versus eukaryotes fuchs (2006)...

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


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


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


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


Tree of life: the genomic perspective (II)

Ciccarelli et al. (2006) Fig. 2

Archaea

Eukaryota

Bacteria


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


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


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


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)


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


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


Timing and ecological context of eukaryote origins: classical view


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


Timing and ecological context of eukaryote origins: critical view


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)


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


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


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)


Acquisition of plant-like genes in trypanosomes

Martin and Borst (2003) PNAS 100:765-767

master microbiology evolution of the eukaryotic cell · prokaryotes versus eukaryotes fuchs (2006)...

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