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Mitochondria. Molecular evolution of the mitochondrial genome. Mitochondria. The powerhouse of eukaryotic cells. The powerhouse of eukaryotic cells. The powerhouse of eukaryotic cells. The powerhouse of eukaryotic cells. Anderson et al. 1981 Nature 290, 457 - 465. ABSTRACT

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mitochondria

Mitochondria

Molecular evolution of the mitochondrial genome

anderson et al 1981 nature 290 457 465
Anderson et al. 1981 Nature 290, 457 - 465

ABSTRACT

“The complete sequence of the 16,569-base pair human mitochondrial genome is presented. The genes for the 12S and 16S rRNAs, 22 tRNAs, cytochrome c oxidase subunits I, II and III, ATPase subunit 6, cytochrome b and eight other predicted protein coding genes have been located.”

anderson et al 1981 nature 290 457 4658
Anderson et al. 1981 Nature 290, 457 - 465

ABSTRACT (continue)

“The sequence shows extreme economy in that the genes have none or only a few noncoding bases between them, and in many cases the termination codons are not coded in the DNA but are created post-transcriptionally by polyadenylation of the mRNAs.”

human mitochondrial genome
Human mitochondrial genome

H-strand

(Heavy strand)

16,569

base pairs

L-strand

(Light strand)

Anderson et al. 1981 Nature290, 457 - 465

slide10

Nucleus or mitochondria

Mitochondria

Nucleus

Burger et al. TRENDS in Genetics Vol.19 No.12 December 2003

conclusion1 mitochondrial proteins
Conclusion1:Mitochondrial proteins
  • There are more protein in the mitochondria than those encoded in the mitochondrial genome
  • The mt proteins that are not encoded in the genome are imported from the nucleus
  • The mitochondrial genome is different between species
animal mitochondrial genomes
Animal mitochondrial genomes

The main difference is usually gene order.

Control region

variation in genes order bird genome

T

P

ND6

E

CR

F

cyt b

12S

T1

P1

ND61

E1

CR1

T2

P2

ND62

E2

CR2

F

cyt b

12S

Variation in genes orderBird genome

Ancestral gene order (chicken)

Hypothetical intermediate stage (albatrosses)

xxxxxxxxxxxxxx

xxx

xxxxx

Derived gene order (crow)

P

ND6

E

NC

T

CR

F

cyt b

12S

molecular tree
Molecular tree

Porifera

Cnidaria

Plathyelminthes

Lophotrochozoa

Annelids

Mollusca

Arthropodes

Ecdysozoa

Nematodes

Echinodermata

Chordata

eukaryotes mitochondrial genome anything goes

Amoebidium

(Ichthyosporean)

Spizellomyces (Fungi)

Tetrahymena (Ciliate)

Eukaryotes mitochondrial genome: anything goes !!!

Homo (Metazoa)

After Burger et al. 2003

mitochondrial genome content
Mitochondrial genome content

Homo

(Metazoa)

genes

Arabidopsis

(Viridiplantae)

introns

non coding

mitochondrial intron
Mitochondrial intron
  • There is no spliceosome in the mitochondria. (a spliceosome is a complex of specialized RNA and protein subunits that removes introns from a transcribed pre-mRNA).
  • Mitochondrial introns are catalytic introns are large self-splicing ribozymes. They catalyze their own excision from mRNA, tRNA and rRNA precursors.
  • There are two self-spicing intron types: Group I and Group II introns.
slide20

Secondary structureof type 1intron

Tetrahymena thermophilus

26S

26S

slide23

group III introns

are present in

eukaryotic nucleus

reclinomonas
Reclinomonas

Genus of small bacterivorous zooflagellates. The single species, R. americana Flavin & Nerad, 1993, is known from freshwater and soil habitats in the United States of America and New Zealand.

conclusion2 mitochondrial genome
Conclusion2:Mitochondrial genome
  • The genome shape and content is different between Eukaryotes lineages
  • There were independent gene losses in the different Eukaryotes lineages
  • The genome evolve via duplications, deletions, and inversion,
  • Gene order can help to reconstruct the evolutionary relationships
18s rrna tree
18S rRNA tree

[TREE vol. 13, no. 12 December 1998]

microsporidia
Microsporidia

Microsporidia are anaerobic protists. They are unusual in lacking mitochondria.

trichomonads
Trichomonads

The trichomonads are an order of anaerobic protists. Most are either parasites or other endosymbionts of animals

Trichomonas

vaginalis

diplomonads
Diplomonads

The diplomonads are a group of flagellates protists, most of which are parasitic. Most diplomonads are double cells: they have two nuclei, each with four associated flagella. They lack both mitochondria and Golgi apparatus.

Giardia lamblia

18s rrna tree33
18S rRNA tree

[TREE vol. 13, no. 12 December 1998]

long branch artifact lba

A

B

=

C

Outgroup

Reconstructed tree

B

A

A

C

=

B

Outgroup

C

Outgroup

Long Branch Artifact (LBA)

True tree

A

B

C

Outgroup

100

conclusion3 mitochondria and eukaryotes
Conclusion3:Mitochondria and Eukaryotes
  • Eukaryotes without mitochondria have never exited (Archeozoa)
  • Eukaryotes without mitochondria have lost their mitochondria (they usually have mitosomes or hydrogenosomes)
slide39

Ehrlichia ruminantium

Ehrlichia canis

Anaplasma phagocytophilum

Anaplasma marginale

Rickettsiales

Wolbachia pipientis

Neorickettsia sennetsu

Rickettsia sibirica

Rickettsia akari

Rickettsia prowazekii

Arabidopsis thaliana

Reclinomonas americana

Monosiga brevicollis

Mitochondria

Caenorhabditis elegans

Homo sapiens

Saccharomyces cerevisiae

Neurospora crassa

Rhizobium leguminosarum

Agrobacterium tumefaciens

50/

1.0

Sinorhizobium meliloti

Alpha-proteobacteria phylogenetic tree based on

rpoB,atpD, cox2, cox3, and cob sequences

Mesorhizobium loti

Rhizobiales

68/1.0

Brucella melitensis

Rhodopseudomonas palustris

Bradyrhizobium japonicum

Silicibacter pomeroyi

56/0.95

67/1.0

Jannaschia sp. CCS1

67/

1.0

Paracoccus denitrificans

Rhodobacterales

Rhodobacter sphaeroides

74/1.0

Hyphomonas neptunium

73/

1.0

Caulobacter crescentus

Caulobacterales

Zymomonas mobilis

Sphingomonadales

Novosphingobium aromaticivorans

Micavibrio sp. EPB

Magnetospirillum magnetotacticum

58/0.77

Rhodospirillales

Rhodospirillum rubrum

Gluconobacter oxydans

Desulfovibrio desulfuricans

69/1.0

Delta-

Proteobacteria

Geobacter metallireducens

Myxococcus xanthus

Bdellovibrio bacteriovorus

Bacteriovorax marinus

0.1

rickettsiales
Rickettsiales
  • The Rickettsiales, are an order of small proteobacteria. Most of them are endosymbionts or parasites of other cells.
  • Like many obligate, intracellular, microbial pathogens, they have small genomes of (<1.5 Mb) as a result of reductive genome evolution.
conclusion3 mitochondria and bacteria
Conclusion3:Mitochondria and Bacteria
  • Mitochondria are proteobacteria and probably the sister clade of Rickettsiales.
  • Mitochondrial genome < 400 kbp
  • Rickettsiales genomes > 1,000 kbp
slide42

Genome size comparisons

Lang et al. 1999 Annual Review of Genetics vol. 33: 351-397

question
Question
  • Where Did All the Mitochondrial Genes Go?
1 gene loss
1- Gene loss
  • Gene loss from mtDNA appears to be an irreversible process because there are no indications (introns excepted) of widespread and substantial gene flux between mtDNAs of different species or from other genomes to mtDNA.
    • Few exceptions….
muts in coral sarcophyton
MutS in Coral (Sarcophyton)

[J Mol Evol (1998) 46:419–431]

slide46

MutS in Coral (Sarcophyton)

Nuclear encoded

DNA which is involved in mt DNA repair

NJ tree using Dayhoff distance

[J Mol Evol (1998) 46:419–431]

other genes that migrate to the mitochondrial genome
Other genes that migrate to the mitochondrial genome
  • Chloroplast-like tRNA genes in angiosperm (flowering plant) mtDNA.
  • Plasmid-derived DNA and RNA polymerase genes in fungal, plant, and several protist mtDNAs.
  • Mitochondrial introns.
  • ALL OTHER GENES WERE DERIVED VERTICALLY from the proto-mitochondrial ancestor
gene loss
Gene loss
  • Genes whose function became obsolete in the setting of a specialized organelle, such as those involved in nucleotide, lipid, and amino acid biosynthesis, must have been eliminated from most mtDNAs early on in evolutionary history.
question49
Question
  • Where Did All the Mitochondrial Genes Go?
2 take over of the corresponding function by nuclear genes
2- Take-over of the corresponding function by nuclear genes
  • For example, in the ciliate protozoans Tetrahymena pyriformis or the cnidaria, the mtDNA encodes, respectively, only seven and two distinct tRNA genes.
  • To ensure translation of all codons in mitochondrial protein-coding genes, missing mitochondrial tRNAs are imported from the cytosol (proven only in the ciliate).
few trna in coral mt genomes
Few tRNA in coral mt genomes

Metridium

After Beagley et al. 1998

question53
Question
  • Where Did All the Mitochondrial Genes Go?
3 mt genes migrated to the nucleus

rns

rnl

G

V

cox2

F

247

A

I2

Y1

nad5

K

atp8

atp6

R2

R1

cox3

nad2

Q

W

A

L1

I1

N

L2

cob

nad1

T

atp9

C

S1

271

S2

P

nad4

cox1

H

Y2

E

D

nad6

nad4L

364

nad3

3- Mt genes migrated to the nucleus

ATP synthase

subunit 9

slide55

Nucleus or Mitochondria

Mitochondria

Nucleus

Complex 5

ATP synthase

Burger et al. TRENDS in Genetics Vol.19 No.12 December 2003

atp synthase
ATP synthase

The ATP synthase is a large protein complex with a proton channel that allows re-entry of protons.

atp subunit 9 story
ATP subunit 9 story
  • In human and other animals ATP 9 is encoded in the nuclear genome.
  • In most fungi, plants, and protists ATP 9 is encoded in the mitochondrial genome.
metazoa phylogenetic tree
Metazoa phylogenetic tree

Bilateria

Nuclear

ATP9

Coral

Sponges

Mitochondrial

ATP9

Fungi

slide59

There is no

ATP9 gene !!

how to explain the evolution of atp9 in animal
How to explain the evolution of ATP9 in animal ???

Bilateria

Coral

Negombata

Tethya

Axinella

Sponges

Geodia

Amphimedon

Oscarella

Iphiteon

Sympagella

Fungi

how to explain the evolution of atp9 in animal61
How to explain the evolution of ATP9 in animal ???
  • There was independent transfer of ATP 9 to the nuclear genome.
cox 2 in plants
Cox 2 in plants
  • For example, in leguminous plants, the active gene coding for cytochrome oxidase subunit 2 (cox2) is nuclear in some species, whereas in other taxa (as in all other plants), cox2 is mtDNA-encoded. In soybean, an inactive mitochondrial gene copy has been detected in addition to an active nuclear one, whereas this gene has been completely eliminated from the mtDNA of cowpea, a close relative.
conclusions
Conclusions
  • We can find that some mt genes migrate to the nuclear genome, when some species have the gene in their mitochondrial genome while other have the same genes encoded in their nuclear genome.
  • What about mt genes that migrated to the nuclear genome in the ancestor of eukaryotes?????
hsp 70
HSP 70

The 70 kilodalton heat shock proteins are a family of ubiquitously expressedproteins. Proteins with similar structure exist in virtually all living organisms. The Hsp70s are an important part of the cell's machinery for protein folding, and help to protect cells from stress.

Gupta and Singh Current Biology (1994) 4:1104-1114

hsp 7065
HSP 70

Human_cyt

Yeast_cyt

Cytoplasm

Bacteria

Maize_cyt

Plant

Giardia_cyt

Animal

Human_er

Endoplasmic

reticulum

Yeast_er

Giardia_er

Chloroplast

Pea_chl

Synechosystis

Drosophila_mt

Mitochondria

Yeast_mt

E.coli

Other_Bacteria

Many_Bacteria

Archae

conclusions66
Conclusions
  • Some genes that are encoded in the nucleus and expressed in the mitochondria are remnant of the ancestral mitochondrial genome.
  • What about eukaryotes without mitochondria?
valrs tree
ValRS tree

Hashimoto, Tetsuo et al. (1998) PNAS 95, 6860-6865

aminoacyl trna synthetase
Aminoacyl-tRNA synthetase

Aminoacyl-tRNA synthetases covalently link an amino acid to a a tRNA, that contains the triplet anti-codon for that amino acid

valrs indel
ValRS indel

TV= Trichomonas

GL=Gardia

37 amino-acid gap

Hashimoto, Tetsuo et al. (1998) PNAS 95, 6860-6865

remark about indel and phylogeny

----------

ASRSGFGGSGGGRGGASGPG

MPGGGASAASGRLLTAAE

----------

ASRSGFGGSGGGRGGASGPG

MPGGGASAASGRLLTAAE

Remark about INDEL and phylogeny
  • INDEL=insertion deletion (also called GAP)

A

MPGGGASAASGRLLTAAEQRGSREAAGSASRSGFGGSGGGRGGASGPG

B

MPGGGASAASGRLLTAAEQRGSREAAGSASRSGFGGSGGGRGGASGPG

C

MPGGGASAASGRLLTAAEQRGSREAAGSASRSGFGGSGGGRGGASGPG

E

D

outgroup

MPGGGASAASGRLLTAAEQRGSREAAGSASRSGFGGSGGGRGGASGPG

Indel: rare changes as phylogenetic markers

indels to solve phylogeny
Indels to solve phylogeny
  • Gupta et al (2005) showed that it is possible to use indels and protein signatures to solve phylogeny of bacteria.
valrs indel72
ValRS indel

TV= Trichomonas

GL=Gardia

37 amino-acid gap

Hashimoto, Tetsuo et al. (1998) PNAS 95, 6860-6865

cpn60 tree
cpn60 tree

Nuclear encoded

Rickettsiales

Roger, Andrew J. et al. (1998) Proc. Natl. Acad. Sci. USA 95, 229-234

conclusions74
Conclusions
  • We can find that some genes of mitochondrial origin in the genome of amitochondriate eukaryotes which indicate that they once had mitochondria.