déclin et contingence, bases de l'évolution biologique
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AAAATTTTCGTATCTGTTGGAGTTAGATAAGCCTACGCTTGATGGACCGTTGGGTGGCTTTCTAAGTGAGCTCGTGCCATCACAATTAATATAAGGAATTGTAGATGTTTCTTTCGTTATAGGTATTTCAA
AATAATTATAAGAACCTACGCCCTCGTCTTTCTCCATTGGAACAGTTGCCGTTTTCGCAGTTCTTTTTGGTTCAGTCCTCATATCATGTGATTCCCCTGGCTCTCCTGATCTTTTTATACTTACTTTGAAAT
CGTCATATGTGTATTTCTTTGATGCAACTCCGATAACGAAGACAATGCTTCCAATAATAACTAAGAATTTGCATACCGTTATTAAACCTACCAAAAGTTTACCTATAAGCTTCTGTAATATTGGCCCCATCA
TTGTTGTGAATACGCACCCTACCAAAAATGATGGGAAATCCAGCACAATACTGCCAGGCCCACTACCTATTGTAATTTTCCATCGTAACCAATCCCTTTTCAAATCCATCCGTGACTTCTATGTCTCGTTA
CTTTCACAGCGTGTGGAGCTACTAGAAAAGTGGCAAAGCTAAACAGCTGATCGAAGTAAACAGAAAAGAACACTAATTGTAGATCAGGCTGTGTACTAGACCTTATTTTACTGTATTTTTTCGGAAAGAA
AAAAGGAGCGCTTTGCAGATCGAAAGTTTCGCTCGTAAATTATTTGTAAGATGCTATTCATAATATGTTAACTGAGAGAAACCAGGTCAAAACAAAACAATTTTGGGCTCTTGCCTCCAAATTTGCCTACC
CTAGAACAGGTATCCATTATCTCGCCTGTACCCGATTAAAAAAAAGACCAATTATTTAAAACTTCTCAAGAAGTTTCATATGCAGTGTATAAGTTGAAGGAATATAGGAATATATATCCTTCAGAAAAGCA
ACACAATACCTAATTACATAACCGATATTTACCTTTTAGAGTGCCTCATTCTTGCAATCTTTCTGTTCGCCATAACACCACCGCCCATGCTCATGCCATTATTTGTTCCCATCCCCATCTGATTAGGGGCT
GACTGCGGCTGCCCAAAAGAAGTTGTCGGCACACCACCTGCCCCCCCAAAAATGGATGATGGATTTGTTACGTTTGAATTGGAACCAGAGGCAGCATTCGCACCAAATATATCACTTGGCCTTAATGC
ATTGGTCGCGGTATTAGTAATTCCGCCATTCAATCCGCTAAAATTAATATTAGGAACTGTTGATGGCGTGAATGAGCTGTTTGTATTGAAAGATGGGGTTTGCGATTGATGTGGTTGGTTATTAGAGCCG
GCAAACACCGTATTAGCATTAGTGTTGCCGTTCATATTAAATACAGAGCCGCCACCAGGCGTTGAATTATTTCCCGTAAAATTAAAAGCAGAGGGAACATTGACATTTTGTGCATTCGTGGAAGGAGGTT
TATTGAATAAACCAGCATTAGCATTAGTTGACGAAGTTGCTGATGTAAAAGGATTGAGACCCCCTGCACCATTGTTTCCAAAATTAAATGAAGATTGATTAGAAGCTGCACCAGTTGCTGCTGTTCCTGA
GCTCGAAAAGCCAAATGCCGAGCCCGCTCCATTCGTATTGCCACTAGCGATACTTTGATCCGGTTTTCCTACGTTAAATGTACCCGCTATATTGGTTCCTGAGGTATTGGAAGTAGTAGTTGTGCCGTT
ACCAGTAGCAGGGGCGTTAAACGAGAATGATGTGGAGTTTGCTGAGGCATTGGTACCATTGGTGTTAGCAGTACCGAATGAAAATGCAGATTTAGATGTTGTATTACCAGTAGCGTCTGTTGGCTTACC
CAAGACAGGAATCGGCGTTGAGGAAGCAGAACCATCGAAGAAAGAAGTTGGAGAGTTTGACTTTTCTTTATTGTGATTGAACTTTGTAAAGGAAAAGCCATTTGATAGCTTCTCCGTATTTGCTGCCGC
TGTACTTGCTGTCGACTTCATCGACTCGGGAGCCCCAAAACTAAAAGATGGTTTTGTGCTAGTGGTTGTTGTATTATTTGTTGTGGAACCGCCAAAGGTGAAAGATGGCGGTGTAGGTCTTTTATCTGT
CTCATTAGCAGGAGGTTTAGTGAAAGAAAATGAGGTGTTAGAGCCTGGTGGTTCTTTAGCTGCATCTGACTTACCAAATGAAAACAATGGCTTTGGTTGTGAGGTTTTTGAAGACGCAAACGTAAAGGA
GGGCTTTTTAGGTTCCGAAACAACAGATGAATCTTTTTGAGCAGGTTCAGTAAAAGAAAAAGTTGGCTTGAGAGTCTTATCATCCGTCGGTGCTTGAACATCAACAGGCTTGCCCGGAAACGAAAACGA
GGGTTTAGCTGCTTCGTTTGAAATTGGACTACTCTTACGTTCCTCCTCTGACTTAGAGAAAGAGAATGTAGGTTTCGCACTTCCCTCAGAGATCTTATTTTCACTTGTTGACTGCCCAAAAGTAAAAGTAG
GCTTCTTGACTATTGTGGCAGGTGTCTCAGATGGTTTGGTGTGTGTTTCTTTCGCGGTGGCGGCTTTACCAAAGGTAAATTGTGCAGAGGAGTCAATATTGCTTGTTACATCAGCTTTTTTTCCGAATGT
AAATAATGGTGTACCTTCAGCTTGCTTATCACTTGCACCAAAGACAAAGCTTGGTTTCCCTGATGCGTCCTTTTCTGACTCTCCCTTTTTGGTCTCCTTTTGATCACCGGTCTTGCCGAAATCGAATAAAG
GCTTGGTGTTTGTATCCTCGCTAACAGGTAAACGCCTTTTTCTTTTGGGCTCATTTTCATCATCACCTTCATCACCATTCTCTTCTTGTTTACCAAAAGAAAATATTGGAGCAGTTGATTTTGGAGGCGCG
TCTGATTCTGTATGATTTTCACTTTTTTCGGATGTCTTTCCAAATTTAAAAGGTTGACTGGCAGAAGTAACGGTATCTGATTTACCACCAAAATTGAATAAAGTTGTGGAAGGGACAGTATTGTCGACAGC
CTTAGTTTTATTAGCCTTTTGGCTAAAATTGAATGATAAGGTAGGCGCCTCGGCAGTTTTCGTTGACTTATCGGTTTTTCCCATTTCTACACTCGATTTAAAGACTGCACCTGCAGAAGAAGTTGCCTTAG
GAGAAGTTTTCTTAGATGGAGTCTCATTGTCCTTGATAAAGTCAAAACCTACGGTGGGCAAAACAATACTTTCTTTGTCCTTTTTGGGCTCAATATTTTTCTTTAACGTAGGCGTACCAGAGCGCTCTGAA
TTGGGAACAAAGCTCTCCTGAATAGGGGCAGTTTTTGCAACTGTGGAAGCTGGTCCTTTTAAAAGTAGATTTTTTTGAGGATTCGATAACCTATTAGAGTTGATGTCTGCACGTAGGTCTTCAATTTCGC
TTGTCAGGTTAGGGCCTGTAGCCAGATTGCCATTTGAAATACTACTCTTAATATTATTTCTATTCTCGCTTGTCTTCTGATCACCGCCAGCGTTACCTTCCTTATCCTTGTTATCCTTTTTTTGTATAGCGT
CATATTCTGACAAATCATATTCAAAATTTGCTGACCACACGGTCCCCTTTGACTGACTATGAAACCTTTTTCTATTGGATCTATTTTTCAATGATTTGAGAATGGGTAGTCCAACATTGGTGTCTTCACCGC
TTTTTCCGGCCAACTGCCTAGTGCAAGAACCGTTTTTAATAGGGGAAGGAGTAGATGATGTGCATAGGTACGATCCTCCCTCATCGCTTTTACTTTGAGAGCCCAATATAACCGACGATGTAATAGATG
GAAATTCAGTTGATTGAATTAATCCAAGCTCACGCATATTTCTCACCCTCTGCTTCTCCCTTAATAACCTCAGTCTTTGAATGGGCAAAATTGGCAAAAGCGGCGGTCTCTCAGTGTTTTCGGTTCCATAT
ATTATAATTGGCGCATTATTGTTGTTCTGAGTTAAGCTGTCGCTATGCTGTGATGTACCGGACACCCTCTTTCTCTTATTAACATGCAGTGTGTCTTCAACATCTGATTCCTCCAAATGATTCGCGTATGA
GAGGTTTGAACTGAAAACTTTCTTGCTCGATGGCCGTTTTTTATTGGGGTTTGTGAAGAATGATTTTAAAGTGGAAGAAAACGATCTCTTTTCGACACGTGGAGAAGACATCACAGAAGAAGTGTTTGAA
GACATGAATGACTAAAAATTGTCGCTCACTCTCTGTCCCTATAACCCTTTCGAGGCTAATATCCTATCGTATTTGCACCGCTACGTAGTGTCCTTATTGAGTTCCTCATCACTTATTTTCTTTAAGTGTTTC
TTGACATTACGAAATTTCGTCAAAGAAAAAAATTAAAATGAAAAAGCATTTCAATGTCACATAATACGAACCATTGATCACGTGCAACGACAAACCCTAAATATAAAAACTAGGGCGTAAAAACCGGGGC
TTGAAAATTAGGGCATAAAATAGGCTTTGCATACACGTGACTTATATTTGGTGTCGGCGTTTTCTTTACGCGGTGTAGTGTAAATCTCTTGTCGTACAAGTGGATATACGCACTGTATACCTCCAGTAACA
CCAAAAAAAAAACCGTGGTTGTCCCATGTAAACGAGTACCGCACACGTAGGCCAAAGCACTCCAGAGAGACTTCGTGTCAAAGGTCTATAATAGGTGGTGCCTTCTTGCTTCTTTTTTGCAGATTCTTA
GTATAATACGCTAGACTATTGTACTTTCTAATTTTAAGAGATATCTTTTTCCTCACAAAGATTTCGTTAAGCAATCGAAGTAAAGTACTCCATCAGAAGAGTTTTTAAAATTTTCGTATCTGTTGGAGTTAGA
TAAGCCTACGCTTGATGGACCGTTGGGTGGCTTTCTAAGTGAGCTCGTGCCATCACAATTAATATAAGGAATTGTAGATGTTTCTTTCGTTATAGGTATTTCAAAATAATTATAAGAACCTACGCCCTCGT
CTTTCTCCATTGGAACAGTTGCCGTTTTCGCAGTTCTTTTTGGTTCAGTCCTCATATCATGTGATTCCCCTGGCTCTCCTGATCTTTTTATACTTACTTTGAAATCGTCATATGTGTATTTCTTTGATGCAAC
TCCGATAACGAAGACAATGCTTCCAATAATAACTAAGAATTTGCATACCGTTATTAAACCTACCAAAAGTTTACCTATAAGCTTCTGTAATATTGGCCCCATCATTGTTGTGAATACGCACCCTACCAAAA
ATGATGGGAAATCCAGCACAATACTGCCAGGCCCACTACCTATTGTAATTTTCCATCGTAACCAATCCCTTTTCAAATCCATCCGTGACTTCTATGTCTCGTTACTTTCACAGCGTGTGGAGCTACTAGA
AAAGTGGCAAAGCTAAACAGCTGATCGAAGTAAACAGAAAAGAACACTAATTGTAGATCAGGCTGTGTACTAGACCTTATTTTACTGTATTTTTTCGGAAAGAAAAAAGGAGCGCTTTGCAGATCGAAAG
TTTCGCTCGTAAATTATTTGTAAGATGCTATTCATAATATGTTAACTGAGAGAAACCAGGTCAAAACAAAACAATTTTGGGCTCTTGCCTCCAAATTTGCCTACCCTAGAACAGGTATCCATTATCTCGCC
TGTACCCGATTAAAAAAAAGACCAATTATTTAAAACTTCTCAAGAAGTTTCATATGCAGTGTATAAGTTGAAGGAATATAGGAATATATATCCTTCAGAAAAGCAACACAATACCTAATTACATAACCGATA
TTTACCTTTTAGAGTGCCTCATTCTTGCAATCTTTCTGTTCGCCATAACACCACCGCCCATGCTCATGCCATTATTTGTTCCCATCCCCATCTGATTAGGGGCTGACTGCGGCTGCCCAAAAGAAGTTGT
CGGCACACCACCTGCCCCCCCAAAAATGGATGATGGATTTGTTACGTTTGAATTGGAACCAGAGGCAGCATTCGCACCAAATATATCACTTGGCCTTAATGCATTGGTCGCGGTATTAGTAATTCCGCC
ATTCAATCCGCTAAAATTAATATTAGGAACTGTTGATGGCGTGAATGAGCTGTTTGTATTGAAAGATGGGGTTTGCGATTGATGTGGTTGGTTATTAGAGCCGGCAAACACCGTATTAGCATTAGTGTTG
CCGTTCATATTAAATACAGAGCCGCCACCAGGCGTTGAATTATTTCCCGTAAAATTAAAAGCAGAGGGAACATTGACATTTTGTGCATTCGTGGAAGGAGGTTTATTGAATAAACCAGCATTAGCATTAG
TTGACGAAGTTGCTGATGTAAAAGGATTGAGACCCCCTGCACCATTGTTTCCAAAATTAAATGAAGATTGATTAGAAGCTGCACCAGTTGCTGCTGTTCCTGAGCTCGAAAAGCCAAATGCCGAGCCCG
CTCCATTCGTATTGCCACTAGCGATACTTTGATCCGGTTTTCCTACGTTAAATGTACCCGCTATATTGGTTCCTGAGGTATTGGAAGTAGTAGTTGTGCCGTTACCAGTAGCAGGGGCGTTAAACGAGAA
TGATGTGGAGTTTGCTGAGGCATTGGTACCATTGGTGTTAGCAGTACCGAATGAAAATGCAGATTTAGATGTTGTATTACCAGTAGCGTCTGTTGGCTTACCCAAGACAGGAATCGGCGTTGAGGAAG
CAGAACCATCGAAGAAAGAAGTTGGAGAGTTTGACTTTTCTTTATTGTGATTGAACTTTGTAAAGGAAAAGCCATTTGATAGCTTCTCCGTATTTGCTGCCGCTGTACTTGCTGTCGACTTCATCGACTC
GGGAGCCCCAAAACTAAAAGATGGTTTTGTGCTAGTGGTTGTTGTATTATTTGTTGTGGAACCGCCAAAGGTGAAAGATGGCGGTGTAGGTCTTTTATCTGTCTCATTAGCAGGAGGTTTAGTGAAAGA
AAATGAGGTGTTAGAGCCTGGTGGTTCTTTAGCTGCATCTGACTTACCAAATGAAAACAATGGCTTTGGTTGTGAGGTTTTTGAAGACGCAAACGTAAAGGAGGGCTTTTTAGGTTCCGAAACAACAGA
TGAATCTTTTTGAGCAGGTTCAGTAAAAGAAAAAGTTGGCTTGAGAGTCTTATCATCCGTCGGTGCTTGAACATCAACAGGCTTGCCCGGAAACGAAAACGAGGGTTTAGCTGCTTCGTTTGAAATTGG
ACTACTCTTACGTTCCTCCTCTGACTTAGAGAAAGAGAATGTAGGTTTCGCACTTCCCTCAGAGATCTTATTTTCACTTGTTGACTGCCCAAAAGTAAAAGTAGGCTTCTTGACTATTGTGGCAGGTGTCT
CAGATGGTTTGGTGTGTGTTTCTTTCGCGGTGGCGGCTTTACCAAAGGTAAATTGTGCAGAGGAGTCAATATTGCTTGTTACATCAGCTTTTTTTCCGAATGTAAATAATGGTGTACCTTCAGCTTGCTTA
TGGTCTCCTTTTG CTTGCCGAAATCGAATAAAG
GTGTTTGTATCCTCGCTAACAGGTAA CGCCTTTTTCTTTTGGGCTCATTTTCATCA
CACCTTCATCACCATTCTCTTCTTGTTTAGGC AAAAGAAAATATTGGAGCAGTTGATTTTGGA
AGGGCGCGTCTGATTCTGTATGATTTTCACG GTTTTTTCGGATGCTCTTTCCAAATTTAAA
GGTTGACTGGCAAGAAGTAACGGTATC TACCACCTTAAAAATTGAATAAAGT
GGGACAGAATTGTCG
TGGTCTCCTTTTG CTTGCCGAAATCGAATAAAG
GTGTTTGTATCCTCGCTAACAGGTAA CGCCTTTTTCTTTTGGGCTCATTTTCATCA
CACCTTCATCACCATTCTCTTCTTGTTTAGGC AAAAGAAAATATTGGAGCAGTTGATTTTGGA
AGGGCGCGTCTGATTCTGTATGATTTTCACG GTTTTTTCGGATGCTCTTTCCAAATTTAAA
GGTTGACTGGCAAGAAGTAACGGTATC TACCACCTTAAAAATTGAATAAAGT
GGGACAGAATTGTCG
ATGGCTTTGG GGTTTTTGAAGAC
ACGTAAAGGAGGTTT AGGTTCCGAAACAA
GAGCAGGTTCAG AAGTTGGCTG
ATGGCTTTGG GGTTTTTGAAGAC
ACGTAAAGGAGGTTT AGGTTCCGAAACAA
GAGCAGGTTCAG AAGTTGGCTG
Bernard Dujon Bernard Dujon
Déclin et contingence, bases de l'évolution
biologique
Decline and contingency, bases of biological
evolution
Déclin et contingence, bases de l'évolution
biologique
Decline and contingency, bases of biological
evolution
Colloque Sciences de la vie, sciences de l'information Centre culturel international de Cerisy-la-Salle, 17-24 Septembre 2016
Ernst Haeckel, 1834 -1919
Unicellular
(without nuclei)
Unicellular
(with nuclei) Pluricellular
1866
2016 Multiple
Reversible
Symbioses
Gregor Johann Mendel, 1822 - 1884
1866
Genotype Phenotype
DNA RNA Proteins 1953 RNA RNA
2016 Gene and allele
interactions Complex RNA
interactions (splicing, editing, processing, RNAi, trans-generational …)
Intrinsic variance
Regular selection acting on limited variations
Charles Robert Darwin
(1809 -1882)
Abrupt genetic changes
Hugo Marie de Vries
(1848 -1935)
?
Species or
individual n° 2
Common core of genes
(ancestral origin)
Species or
individual n° 1
Species or
individual n° 3
Restricted set of genes
(origin ?)
ca. 100 genes mutated and
a few genes missing
CNV in the human genome CNV in the human genome
Yoon et al., (2009)
Genome Res. 19: 1586-1592
Segmental duplications Segmental deletions
Gene losses
Pseudogenes
Deletions
Gene gains
Duplications
Fission / fusion
De novo formation
Horizontal acquisitions
Each genome is only a snapshot in time within
continual changes, not an optimized structure
1: Genomes are (much) too big
2: There are too many genes in genomes
The C-value paradox (Swift, 1950)
Major lessons from genomics Major lessons from genomics
Genomes are too big Genomes are too big
Paramecium
tetraurelia
100 Mb
Gonyaulax
grindleyi
98 000 Mb
1000 X
Zea mais
3 000 Mb
Vitis vinifera
487 Mb
Fritillaria
assyriaca
100 000 Mb
1000 X
Amoeba dubia
670 000 Mb
Homo sapiens
2 900 Mb
Necturus lewisi
100 000 Mb
Saccharomyces
cerevisiae 12 Mb
55 000 X
Genome sizes and content
Coding exons (exome) 1.9 % of genome
Introns
> 100 000
Other
pseudo -genes
~25 000
Regulations and
evolution: 98.1 %
Mobile elements > 1 100 000
Genes are complex mosaics (exons and introns)
Many genes encode RNA, not proteins
Genomes contain many other elements than genes:
- pseudogenes and traces of ancient sequences
- mobile elements and their remnants
- NUMTs, NUPTs, NUPAVs
- structural elements of chromosomes (CEN, TEL)
- transcription is pervasive
UTR and introns Coding exons Mobile elements and remants Pseudogenes DNA RNA
Too many genes in genomes
The genome of Saccharomyces cerevisiae
13.4 Mb (> 70 % coding) ~ 5 800 protein-coding genes
44 % of genes are not unique (paralogs)
Many genes escaped systematic genetic screenings
1996
No genome is minimal
In each genome many genes are dispensible
< 18 % of genes are essential for cellular life
> 50 % of the non-essential genes generate no detectable phenotype when deleted
The yeast systematic gene deletion collection The yeast systematic gene deletion collection
Core and pan-genomes Core and pan-genomes Variability + dispensability --> core- and pan-genomes
Medini et al., 2005 «The microbial
pan-genome» Curr. Op. Genetics & Development 15: 589-594
Closed species: e.g. B. anthracis
Open species: e.g. S. agalactiae
> What is a species ?
From 61 E. coli genomes fully sequenced (Lukjancenko et al., 2010 Microb. Ecol. 60: 708-720)
ca. 4 000 genes / individual genome
pan-genome : 15 574 gene families
core-genome: 993 gene families
Adapted from Wolf and Koonin (2013) Bioessays 35: 829-837
Phase of complexification: brief, sporadic
Phase of reductive evolution: long, nearly clockwise
Burst of novel
lineages
Gradual reductive
evolution in each
lineage
Reductive evolution
Parasitism, commensalism, symbiosis: Microsporidia, Chlorarachniophytes, Cryptophytes
Loss of genes and loss of functions play the key role in evolution
Role of sex, loss of sex and horizontal acquisitions: Bdelloid rotifers
Free-living eukaryotes: Yeasts
Microsporidia Microsporidia
Corradi and Slamovits, 2010,
Brief. Funct. Genomics 10: 115-124.
2001 vol. 414: . 450-453
Genome size: 2.5 Mb
Total genes: 1 997
Microsporidia Microsporidia
Horizontal gene acquisitions in
Encephalitozoon hellem Horizontal acquisition of genes involved in nucleic-acid metabolism
Alexander et al. 2016 PNAS 113: 4116-4121
Complex ancestor Intermediate forms Small number of genes
Large genomes
Final forms Small number of genes
Small genomes
Gene loss
Intron loss
Genome size
reduction
Horizontal
acquistions
Gould, 2012, Nature 492: 46-48
Bigellowiella natans Ancestral rhizaria
Guillardia theta Ancestral chromalveolate
Primary endosymbiosis Secondary endosymbiosis
Ancestral eukaryote
Secondary endosymbiosis Secondary endosymbiosis
Viridiplantae
Unikonts Chromalveolata
Excavata
2 313 84
8
748 5 666
Rhizaria
Keeling et al., 2005 Trends in Ecology and Evolution, 20: 670-676
Genomics of the eukaryotes Genomics of the eukaryotes
Bigelowiella natans
Guillardia theta
Curtis et al. (2012) Nature 492: 59-65
Genome size (Mb) 87.2 94.7
Split CDS (%) 80 86
Mean exons /gene 6.4 8.8
Mean intron size (nuc.) 110 184
Nucleomorph:
3 chromosomes:
196, 181, 174 kb
inverted repeats at
chromosome ends (rDNA, ubiquitin-
conjugating enzyme gene)
Douglas et al., 2001 Nature
410: 1091-1096
Nucleomorph:
3 chromosomes:
141, 134, 98 kb
inverted repeats at
chromosome ends (rDNA, DnaK
pseudogenes)
Gilson et al., 2006 PNAS
103: 9566-9571
Secondary endosymbiosis Secondary endosymbiosis
Example of a genomic quartet of 4
scaffolds
pairs of
ohnologs
alleles of one
ohnolog
Nature (2013) 503: 453-457
Total genome size 244 Mb (including 26 Mb homozygous 2x)
49,300 protein-coding genes
Numerous homologous blocks (colinear regions) forming two groups: - pairs of ohnologs (mean 74 % identity) corresponding to an ancient
genome duplicaton - pairs of alleles (mean 96 % identity) for each member of the pair of
ohnologs. Their coexistence in the same genome forms quartets that, altogether, cover 40 % of the entire genome (---> a locally tetraploid genome)
Asexual metazoa Asexual metazoa World-wide expansion
Survive total desiccation >
genome fragmentation and
regeneration
Asexual reproduction
The genomic structure is incompatible with conventional meiosis
Allelic pairs are found on the same chromosomes
Colinear regions do not extend to entire chromosome scale
Multiple traces of gene conversion between gene copies reassort alleles without meiosis
Multiple traces of horizontal gene acquisition of non-metazoan origin throughout the genome (8%)
Asexual metazoa Asexual metazoa
M M
M M
M M
B B
B B
B B
etc… etc… etc… etc…
M M B B B B M M
etc…
M M B B
B B M M
etc… etc… etc…
What are yeasts ? What are yeasts ?
Generation 0: 1 cell
Generation 1: 2 cells
Generation 2: 4 cells
Generation 3: 8 cells
Generation 100: ~1030 cells (approx. one week of growth)
i.e. ~ 10 trillions of tons = a several centimeters-high crust covering all world continents
Unicellular forms of modern fungi (devoid of fruiting bodies) adapted to rapid and
unlimited clonal proliferation so long as nutrients are available.
Generation 10: 1 024 cells
Generation 20: 1 048 576 cells
Generation 30: ~109 cells
Generation 50: ~1015 cells
Exponential
mitotic growth
Natural yeasts and experimental models Natural yeasts and experimental models
Terrestrial habitats Leaves, roots, trunks
fruits, plant exudates,
insect guts, soils
Saccharomyces, Lachancea,
Naumovozyma, Kluyveromyces,
Kazachstania, Eremothecium,
Schizosaccharomyces …
Aquatic habitats Fresh or saline water,
planctonic or surfaces
of plants and animals
Rhodotorula, Sporobolomyces,
Debaryomyces, Metchnikowia,
Leucosporidium …
Human, animal or plant pathogens or commensals Antagonist effect against various plant diseases Saccharomyces, Candida, Dipodascus, Cryptococcus, Malassezia
Taphrina, Protomyces, Eremothecium, Galactomyces …
Fermentable sugars: fructose, glucose, sucrose, maltose, melibiose, raffinose, lactose …
Oxidative utilization of a very large variety of organic compounds, including: Non-fermentable sugars: xylose, arabinose, ribose, rhamnose, fucose … Non-fermentable alcohols: methanol, ethanol, propanol,
glycerol, erythritol, ribitol, arabitol, mannitol … Amino-sugars: glucosamine, acetyl-glucosamine, galactosamine… Organic acids: lactic,
succinic, citric, malic … Other compounds: acetone, ethyl acetate, glucuronic acid, anthracene …
Need organic Nitrogen (but some species are able to assimilate nitrate or nitrite)
> 1 500 species
The world of yeasts The world of yeasts
flagellated cells
loss of flagellum
Numerous species e.g. Saccharomyces Debaryomyces, Yarrowia
Few species e.g. Schizosaccharomyces
Ascomycota
~ 1000 MYr
Basidiomycota Some species e.g. Rhodotorula
Some species e.g. Cryptococcus
Few species e.g. Malassezia
Recurrent formation of other yeasts
Rare species e.g. Hortea
Approximate number of generations from present
106 108 109 1010 1011 107 1012
human-chimpanzee separation
"Budding yeasts"
"Fission yeasts"
Filamentous fungi
with fruting bodies
Fungi with fruting
bodies
Fungi with fruting
bodies
Fungi with fruting
bodies
«modern» fungi Dikarya
~1500 MYr
~1100 MYr
Microsporidia and «primitive» fungi
Chytridiomycota Glomeromycota Zygomycota Neocallimastigomycota Blastocladiomycota
Origin of Taphrinomycotina
Origin of Saccharomycotina
Yeasts
M M
Mycelium of Ascomycota or Basidiomycota
M M
M M
B B
B B
B B
etc…
~ Linear
growth
mitosis
~ Exponential
growth
etc… etc… etc…
M M B B B B M M
etc…
M M B B
B B M M
etc… etc… etc…
WhatWhat are are yeastsyeasts ?? WhatWhat are are yeastsyeasts ??
Yeast genomes are highly evolved structures that have lost a number of
ancestral features.
Contrary to common intuitive thinking, yeasts are not a homogeneous
group of closely related, evolutionary primitive eukaryotes. They have
emerged recurrently from distinct lineages of more complex fungi.
Saccharomycotina genome signatures Saccharomycotina genome signatures
Ogataea polymorpha Dekkera bruxellensis
Komagataella pastoris Lindnera jadinii (Candida utilis)
Ogataea parapolymorpha Kuraishia capsulata
Methylo
trophs
Saccharomyces uvarum
Candida dubliniensis
Blastobotrys adeninivorans
Yarrowia lipolytica
Nadsonia fulvescens
Eremothecium cymbalariae
Kazachstania exigua Kazachstania servazzii
Lachancea thermotolerans
Lachancea kluyveri
Kluyveromyces lactis
Saccharomyces cerevisiae
Nakaseomyces (Candida) glabrata
Saccharomyces paradoxus Saccharomyces mikatae Saccharomyces kudriavzevii
Naumovozyma castellii
Lachancea waltii
Eremothecium gossypii
Vanderwaltozyma polyspora
Kazachstania africana
Naumovozyma dairenensis
Tetrapisispora phaffi
Sac
char
omyc
etac
eae
Clavispora lusitaniae
Millerozyma sorbitophila
Candida albicans
Meyerozyma guilliermondii
Candida parapsilosis
Candida tropicalis
Scheffersomyces stipitis
Lodderomyces elongisporus Candida orthopsilosis
Spathaspora passalidarum
«C
TG
»
Debaryomyces hansenii
basal
lineages
Zygosaccharomyces rouxii Torulaspora delbruckii
Nakaseomyces bacillisporus
ZT clade
KLE clade
WGD
code
Geotrichum candidum
Gene numbers
4 700 –
6 000
6 100 –
6 400
5 000 –
6 000
6 100 –
6 800
Genome size
9 -
14
12 -
14
12 -
14
12 -
24
Mb
Coding capacity
> 70
> 70
> 70
~ 45
%
Split genes
3 - 5
6 - 7
15
15 -
35
%
Loss of HP1-mediated chromatin modification & Loss of canonical RNAi machinery
Debaryomyces hansenii
Yarrowia lipolytica
Saccharomyces cerevisiae
1115
329
1443
2823
369 85
834
Gene losses Deletions
Pseudogenes
Gene gains Duplications & sub- or neo-functionalization Hybridizations Horizontal acquisitions De novo formation
functional losses associated to gene loss
Sugar utilization GAL7 (UDP transferase), GAL10 (epimerase), GAL1 (kinase), GAL3 (activator), SUC2 (invertase)
Phosphate metabolism PHO3, PHO5, PHO11, PHO12 (acid phosphatases), PHO89 (transporter)
Nicotinic acid biosynthesis BNA1, BNA2 (dioxygenases), BNA4 (monooxygenase), BNA5 (kynureninase), BNA6 (phosphoribosyl transferase), BNA7 (kynurenin formamidase)
Allantoine metabolism DAL1, DAL2 (allantoinases), DAL3 (ureidoglycolate lyase)
Transporters OPT1, OPT2 (oligopeptide-transporters)
Etc …
functional gains associated to gene loss
General
metabolism Nicotinic acid NAD+
External nicotinic acid
permeases
Synthetic enzymes
In C. glabrata, the intracellular concentration of NAD+ depends directly on the external concentration of nicotinic acid
---> regulate specific adhesion to epitheliums (Domergue et al., 2005 Science 308, 866-870)
Eukaryotic-type centrom
eres
Post WGD
ZT clade
CTG
Methylotrophs
Basal
KLE clade
Taphrinomycotina
Poin
t centro
mere
s
Sa
cc
ha
rom
yc
eta
cea
e
> 10 kb
3 A A A A 3 3 3
IR IR
3 3 3 A A 3 3 3
heterochromatin heterochromatin
Point centromeres Point centromeres 3
A
Canonical histone H3
Centromeric histone H3 variant (CenP-A)
3 A 3 3 3 3 3
0.13 kb
CDE I CDE II CDE III Recruitment of plasmid elements
Malik and Henikoff, 2009 Cell 138: 1067-1082
Regio
nal c
entro
mere
s
3
3 – 5 kb
A A A A A 3 3 3 3 3
LTR and Ty remnants IR IR
Loss of classical heterochromatin
modification
Geotrichum candidum
24.8 Mb, 6 804 CDS, 35 % with intron(s).
SpecificallySpecifically RetainedRetained Ancestral Ancestral GenesGenes (SRAG)(SRAG)
Debaryomyces hansenii 113 SRAGs (2.0 %) Amino-acid, carbon metabolism, transport … Geotrichum candidum 263 SRAGs (3.9 %) Transcriptional regulation, cell cycle, cellusose /pectin hydrolysis
… Yarrowia lipolytica 232 SRAGs (3.6 %) Extracellular proteases, oxydo-reduction …
Saccharo mycotina
Pezizo mycotina
Taphrinomycotina
Basidiomycota
Pseudo-orphans with discordant phylogenies
280 genes have no homolog in any sequenced Saccharomcotina, but have homologs in Pezizomycotina and / or Basidomycota 17 correspond to horizontal transfers from filamentous fungi (low sequence divergence with outgroup) 263 correspond to SRAG (same sequence divergence with outgroup as other genes)
X
X
Gene loss
and decay
Evolved form 1
Evolved form 2
Evolved form 3
Etc … Duplications, sub-functionalization, neo-
functionalization, exon-shuffling
accompanied by selection
----- adaptations
Complex ancestor etc…
Novel lineage
Novel lineage
Horizontal gene acquistions
Introgressions
Hybridizations, endosymbiosis
Genome duplication
Exon-shuffling
De novo gene formation
--- major innovations
SummarySummary
Genomes are never minimal
Evolution is mostly reticulate
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