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Blaxter 2022-annotated

The Earth BioGenome Project aims to sequence the genomes of all 2 million named eukaryotic species to create a comprehensive digital library of life on Earth. This initiative seeks to address fundamental questions in evolution, ecology, and conservation by providing whole-genome data that represents the full diversity of life. The project is expected to enhance our understanding of speciation, adaptation, and the interconnectedness of ecosystems, ultimately benefiting various fields including agriculture, medicine, and bioindustry.

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0% found this document useful (0 votes)
9 views9 pages

Blaxter 2022-annotated

The Earth BioGenome Project aims to sequence the genomes of all 2 million named eukaryotic species to create a comprehensive digital library of life on Earth. This initiative seeks to address fundamental questions in evolution, ecology, and conservation by providing whole-genome data that represents the full diversity of life. The project is expected to enhance our understanding of speciation, adaptation, and the interconnectedness of ecosystems, ultimately benefiting various fields including agriculture, medicine, and bioindustry.

Uploaded by

Analice Marianne
Copyright
© © All Rights Reserved
We take content rights seriously. If you suspect this is your content, claim it here.
Available Formats
Download as PDF, TXT or read online on Scribd
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SPECIAL FEATURE:

SPECIAL FEATURE: PERSPECTIVE

PERSPECTIVE
Why sequence all eukaryotes?
Mark Blaxtera,1 , John M. Archibaldb , Anna K. Childersc , Jonathan A. Coddingtond ,
Keith A. Crandalle,f , Federica Di Palmag , Richard Durbina,h , Scott V. Edwardsi,j ,
Jennifer A. M. Gravesk,l , Kevin J. Hackettm , Neil Halln , Erich D. Jarviso,p, Rebecca N. Johnsonq ,
Elinor K. Karlssonr,s , W. John Kresst , Shigehiro Kurakuu,v , Mara K. N. Lawniczaka,
Kerstin Lindblad-Tohs,w , Jose V. Lopezx,y , Nancy A. Moranz , Gene E. Robinsonaa,bb ,
Oliver A. Rydercc,dd , Beth Shapiroee, Pamela S. Soltisff,gg , Tandy Warnowhh , Guojie Zhangii,jj , and
Harris A. Lewinkk,ll
Edited by Joan Strassmann, Washington University in St. Louis, St. Louis, MO; received September 10, 2021; accepted November 1, 2021

Life on Earth has evolved from initial simplicity to the astounding complexity we experience today. Bacteria
and archaea have largely excelled in metabolic diversification, but eukaryotes additionally display abundant
morphological innovation. How have these innovations come about and what constraints are there on the
origins of novelty and the continuing maintenance of biodiversity on Earth? The history of life and the code
for the working parts of cells and systems are written in the genome. The Earth BioGenome Project has pro-
posed that the genomes of all extant, named eukaryotes—about 2 million species—should be sequenced to
high quality to produce a digital library of life on Earth, beginning with strategic phylogenetic, ecological,
and high-impact priorities. Here we discuss why we should sequence all eukaryotic species, not just a repre-
sentative few scattered across the many branches of the tree of life. We suggest that many questions of evo-
lutionary and ecological significance will only be addressable when whole-genome data representing
divergences at all of the branchings in the tree of life or all species in natural ecosystems are available. We
envisage that a genomic tree of life will foster understanding of the ongoing processes of speciation, adapta-
tion, and organismal dependencies within entire ecosystems. These explorations will resolve long-standing
problems in phylogenetics, evolution, ecology, conservation, agriculture, bioindustry, and medicine.
genome j diversity j ecology j evolution j conservation

a
Wellcome Sanger Institute, Hinxton, Cambridge CB10 1SA, United Kingdom; bDepartment of Biochemistry and Molecular Biology, Dalhousie
University, Halifax, NS B3H 4H7, Canada; cBee Research Laboratory, Agricultural Research Service, US Department of Agriculture (USDA),
Beltsville, MD 20705; dGlobal Genome Initiative, National Museum of Natural History, Smithsonian Institution, Washington, DC 20560;
e
Computational Biology Institute, Department of Biostatistics and Bioinformatics, George Washington University, Washington, DC 20052;
f
Department of Invertebrate Zoology, Smithsonian Institution, Washington, DC 20013; gSchool of Biological Sciences, University of East Anglia,
Norwich NR4 7TJ, United Kingdom; hDepartment of Genetics, University of Cambridge, Cambridge CB2 3EH, United Kingdom; iDepartment of
Organismic and Evolutionary Biology, Harvard University, Cambridge, MA 02138; jMuseum of Comparative Zoology, Harvard University,
Cambridge, MA 02138; kSchool of Life Sciences, La Trobe University, Bundoora, VIC 751 23, Australia; lUniversity of Canberra, Bruce, ACT 2617,
Australia; mCrop Production and Protection, Office of National Programs, Agricultural Research Service, USDA, Beltsville, MD 20705; nEarlham
Institute, Norwich, Norfolk NR4 7UZ, United Kingdom; oLaboratory of the Neurogenetics of Language, The Rockefeller University, New York, NY
10065; pHoward Hughes Medical Institute, Chevy Chase, MD 20815; qNational Museum of Natural History, Smithsonian Institution, Washington,
DC 20560; rBioinformatics and Integrative Biology, University of Massachusetts Medical School, Worcester, MA 01605; sBroad Institute of MIT
and Harvard, Cambridge, MA 02142; tBotany, National Museum of Natural History, Smithsonian Institution, Washington, DC 20013-7012;
u
Department of Genomics and Evolutionary Biology, National Institute of Genetics, Mishima, Shizuoka 411-8540, Japan; vLaboratory for
Phyloinformatics, RIKEN Center for Biosystems Dynamics Research, Kobe, Hyogo 650-0047, Japan; wScience for Life Laboratory, Department of
Medical Biochemistry and Microbiology, Uppsala University, Uppsala 751 23, Sweden; xDepartment of Biological Sciences, Halmos College of
Arts and Sciences, Nova Southeastern University, Dania Beach, FL 33004; yGuy Harvey Oceanographic Center, Dania Beach, FL 33004;
z
Integrative Biology, University of Texas at Austin, Austin, TX 78712; aaCarl R. Woese Institute for Genomic Biology, University of Illinois at
Urbana–Champaign, Urbana, IL 61801; bbDepartment of Entomology, University of Illinois at Urbana–Champaign, Urbana, IL 61801;
cc
Conservation Genetics, Division of Biology, San Diego Zoo Wildlife Alliance, Escondido, CA 92027; ddDepartment of Evolution, Behavior and
Ecology, University of California, San Diego, La Jolla, CA 92039; eeDepartment of Ecology and Evolutionary Biology, University of California,
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Santa Cruz, CA 95064; ffFlorida Museum of Natural History, University of Florida, Gainesville, FL 32611; ggBiodiversity Institute, University of
Florida, Gainesville, FL 32611; hhDepartment of Computer Science, University of Illinois at Urbana–Champaign, Urbana, IL 61301; iiVillum Center
for Biodiversity Genomics, Section for Ecology and Evolution, Department of Biology, University of Copenhagen, Copenhagen 2100, Denmark;
jj
China National Genebank, Beijing Genomics Institute–Shenzhen, Shenzhen 518083, China; kkDepartment of Evolution and Ecology, College of
Biological Sciences, University of California, Davis, CA 95616; and llDepartment of Population Health and Reproduction, University of California,
Davis, CA 95616
Author contributions: M.B., J.M.A., A.K.C., J.A.C., K.A.C., F.D.P., R.D., S.V.E., J.A.M.G., K.J.H., N.H., E.D.J., R.N.J., E.K.K., W.J.K., S.K.,
M.K.N.L., K.L.-T., J.V.L., N.A.M., G.E.R., O.A.R., B.S., P.S.S., T.W., G.Z., and H.A.L. wrote the paper.
The authors declare no competing interest.
This article is a PNAS Direct Submission.
This open access article is distributed under Creative Commons Attribution License 4.0 (CC BY).
1
To whom correspondence may be addressed. Email: mb35@sanger.ac.uk.
Published January 18, 2022.

PNAS 2022 Vol. 119 No. 4 e2115636118 https://doi.org/10.1073/pnas.2115636118 j 1 of 9


Outcomes of the Earth BioGenome Project

Conservation
Protect
Focus of genomics expands to
biodiversity &
embrace all species, changing how
we analyze their characteristics and mitigate effects
interactions, and their capacity to of climate
adapt to rapid ecological change. change

Ecosystems
Ecological and genomic data are
Support
integrated for all species, uncovering
coevolutionary relationships and ecosystem
interactions in natural and services
human-dominated ecosystems.

Symbiosis
By studying all participants in symbiotic Build pandemic
relationships, unexpected connections security and
between pests, parasites, and mutualist enhance human
symbionts, including physiological health
dependencies, are discovered.

Speciation
Improve
Completely sequenced lineages
agricultural
reveal diverse speciation processes,
from complete separation to ongoing yields & facilitate
hybridization, and underlying genome climate
variation. adaptation

Origins of novelty
Enable
Surveying little studied pockets of
synthetic biology
cellular diversity reveals how basic
processes of life evolved, and uncovers and spur
genes, proteins, and metabolic biotechnological
pathways. innovation

Fig. 1. Outcomes of the Earth BioGenome Project. Sequencing all eukaryotic life on Earth will transform our understanding of how life evolved,
help us build a sustainable future, provide biosecurity, and support an innovative bioeconomy. Here, we summarize the impact of these new
genomes on basic research, which is described in detail in the text. Some practical benefits of this project are captured in the gray circles.

“ … every scrap of biological diversity is priceless, to DNA sequence data, have revealed the outline of the tree of
be learned and cherished, and never to be surren- life, but many of the details are yet to be discovered (6). Each
dered without a struggle.” species is a unique evolutionary experiment, the daughter of an
E. O. Wilson (1) unbroken lineage of successful experiments. To date, much of
comparative genomics has centered on deep analysis of a short
Humans have classified the organisms of the natural world
roster of species, focused around Homo sapiens. While this
into groups by form and utility. In On the Parts of Animals, Aris-
work has revealed many of the details of our and other species’
totle (2) considered both form and function of animal organs
functioning and evolutionary history, each new genome has
and systems to ascertain deeper relationships between kinds.
brought new insights and it is clear that our knowledge is lim-
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The flowering of scientific classification in the 300 y since Lin-


ited to a small part of life’s true diversity (7). If we had the
naeus (3) has given universal names to about 2 million eukary-
genomes of all species, we could ask questions across all spe-
otic species (https://www.catalogueoflife.org/*). The Linnaean
cies: What genes are unique to each group, or ecosystem, or
project is not yet finished, as estimates of true eukaryotic diver-
process? How do genes and genomes change over time and
sity predict over 8 million extant species (4). Elucidation of the
space? What are the rules of evolution on grand and local
processes of evolution and speciation since Darwin’s The Origin
scales? What diversity do we not know, and cannot currently
of Species (5) demonstrates the interconnectedness of all life.
predict?
Molecular characters, and especially phylogenetic analyses of
The answers to these questions represent a quest for omni-
science in biology—a quest to understand nature by character-
*Currently 2,005,428 species; from Species 2000 & ITIS (89). izing its very essence, the DNA that encodes the basic blueprint

2 of 9 j PNAS Blaxter et al.


https://doi.org/10.1073/pnas.2115636118 Why sequence all eukaryotes?
of every species on Earth. This is the goal of the Earth BioGe- Sequence Database Collaboration databases (21) for 0.5 million
nome Project (EBP), a global effort to sequence the genomes species-level taxa,‡ very few sequences are available for most
of all currently named eukaryotic species (8, 9). In this article, species and the overlap of homologous genes between species
we address fundamental reasons for sequencing all species is low. Genome sequences have been used to explore the ori-
(10), and pose sets of questions that can be addressed with gins of eukaryotes and in revising the deep splits in protists,
large numbers of eukaryotic genomes across all clades. A digi- plants, and animals (22–25), but genomes, most in draft form,
tal library of eukaryotic genomes will form the fundamental are available for only 0.4% of all species (9). In particular, the
infrastructure for the future of biology, agriculture, medicine, root of the tree and the placement of the many deep lineages
synthetic biology, and biomaterials science—a foundational of single-celled eukaryotes (the polyphyletic “protists”) remain
legacy that democratizes and enables the science of the future unresolved (24). An accurate description of the tree of life will
(Fig. 1). enable many deep questions about the evolution of eukaryotes
to be definitively addressed (26), such as:
Sequencing All Eukaryotic Life
• What is the complete and true structure of the tree of
The EBP and its affiliated projects† propose the genome
eukaryotes?
sequencing and annotation of all eukaryotic species (8). Each
• How is adaptive radiation reflected in genome structure and
EBP-affiliated project has a different focus, be it geographic,
content, and are these radiations resolvable?
ecosystem, or taxonomic, but they share the goal of produc-
• How common and how important have hybridization and pol-
ing high-quality reference genome assemblies. We aspire,
yploidization been across the tree of life, and what signatures
whenever technically possible, to generate complete genome
have ancient hybridization, polyploidization, and introgression
sequences that span each chromosome of the nuclear genome,
left in genomes?
and include all organellar genomes. The EBP aims to finish
• When, where, and how do new genes arise? Are there pre-
each species’ genome to a quality that will stand the tests of
dictable patterns of gene family origin and diversification in
future science. This exacting standard is achievable using cur- different lineages?
rent long-read and long-range sequencing technologies, and • How important is horizontal gene transfer in the evolution of
using new bioinformatics toolkits designed to exploit the emer- eukaryotes?
gent properties of these exquisitely accurate data (11, 12).
The daunting task of sequencing ∼2 million species is made Having all genomes will allow us to generate well-supported
tractable by focused campaigns to address particular issues of hypotheses of the origins and diversification of all branches of
interest. For example, the Vertebrate Genomes Project aims to the eukaryotic tree, mapping reticulation events and timing of
sequence all 70,000 vertebrate species, but has started with gene duplication, divergence, and loss. Complete genome
reference genomes for each taxonomic order (12). The Darwin sequences are more likely to contain information concerning
Tree of Life Project aims to sequence all 70,000 species in nodes, processes, or events of interest. Complete sequences
Britain and Ireland, and has started with a reference genome will permit rational choice of data to fit questions, for example
for each of the 4,200 taxonomic families represented (13). choosing subsets with divergence rates that match the phylo-
Other projects focus on species and ecosystems that are genetic depth of the nodes being assessed. Full inventories of
iconic for conservation, socially or scientifically important, or families of homologous genes, their protein sequences, and
interesting because of their unique sets of adaptations. By noncoding regulatory elements will highlight divergence and
close coordination under the EBP international network of constraint in functional DNA, RNA, and amino acid residues,
networks, in particular developing platforms and processes and inform bioengineering of new functions. It is clear that
that ensure synergy rather than conflict and promote diversity analyzing many thousands of whole genomes will require
of target selection across life, the expertise and experience method development in orthology and phylogenetic infer-
of thousands of scientists will be brought to bear on this ence toolkits.
“moonshot for biology.”
Defining the Origin of Eukaryotic Cells
Discovering the Trees of Life Understanding the origin of the eukaryotic cell from prokaryotic
Correct phylogenetic trees are essential data for the under- precursors is one of the grand challenges of evolutionary biol-
standing of the origins and diversification of phenotypes. ogy. We still know relatively little about the antecedents of
Dependent inferences will be unreliable if these trees are in eukaryotic cellular complexity and the environmental and selec-
error or unresolved. Should we even be thinking exclusively in tive factors involved. Comparative cell biology and genomics
terms of bifurcating trees (14, 15)? Hybrid origin of new plant tell us that the common ancestor of all known extant eukaryotes
species is common and hybridization, polyploidization, and hor- had a nucleus, temporospatially separated transcription and
translation, a mitochondrion, linear chromosomes, meiotic sex,
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izontal gene transfer have also played major roles in diversifica-


mitosis, an endomembrane and protein trafficking system, and
tion of other clades (16–19). Even without hybridization, gene
a flagellum (27, 28). Homologs of many of the individual pro-
trees across the genome commonly differ from the overarching
teins involved in these diverse machineries and compartments
species tree due to incomplete lineage sorting and the stochas-
can be found in bacteria and archaea—in particular the recently
ticity of genetic drift (20). Existing sequence data have been
discovered Asgard archaea (29, 30)—but precisely how, when,
used to build estimates of the tree of life at global and local
and in what order they evolved is still far from clear. The origin
scales, and this has resolved many questions. However, while
sequence data are available in the International Nucleotide ‡
Value from https://www.ncbi.nlm.nih.gov/Taxonomy/taxonomyhome.html/
index.cgi?chapter=statistics&uncultured=hide&unspecified=hide; including

https://www.earthbiogenome.org/institutional-members and https://www. sequences from strains and isolates without a formal species name increases
earthbiogenome.org/affiliated-project-networks. the count to ∼1.4 million.

Blaxter et al. PNAS j 3 of 9


Why sequence all eukaryotes? https://doi.org/10.1073/pnas.2115636118
of eukaryotes involved endosymbiotic assimilation of the bacte- • How much does coevolution between larger host organisms
rial ancestors of the mitochondrion and, in photosynthesizing and their microbiomes drive diversification?
lineages, the plastid (31, 32). This is analogous to many extant
Access to the genomes of symbiotic partners of all eukary-
mutualist symbiotic systems, where a smaller partner, prokary-
otic species will enable discovery of novel genes and regulatory
otic or eukaryotic, exists engulfed and reliant on a larger eukary- mechanisms that underlie the integration of distinct organisms,
otic host. Fundamental questions about the evolutionary origin
the opening of new ecological niches, and the promotion of
of eukaryotic cells can be addressed with a complete set of
species diversification. Understanding the relative evolutionary
eukaryotic genomes, such as: trajectories of hosts and their smaller partners will deliver under-
• What genes were present in the ancestor of all extant standing of the necessary linkage between these organisms,
eukaryotes? and may lead to directed enhancement of symbioses that bene-
• Did eukaryotic cellular complexity evolve in a stepwise fashion fit society or the environment. Understanding the essential
or all at once? physiological dependencies of pests and parasites and their
• To what extent do present-day symbiotic processes model mutualistic symbionts may also lead to novel intervention
those acting at the origin of eukaryotes? strategies.
• What genomic processes limit and promote the horizontal spread
of photosynthesis by secondary and tertiary endosymbioses? Decrypting Chromosome Evolution
Most bacteria and archaea have single, circular genomes and
Transformative insights into the origin of the eukaryotic cell
are haploid, but the genomes of most eukaryotes are diploid
are most likely to come from sequences of currently unknown
and organized in linear chromosomes. Eukaryotic chromatin is
pockets of cellular diversity within the archaeal and microbial
folded into a three-dimensional (3D) conformation that is critical
eukaryotic domains, recognizing that key intermediates may
to gene expression and cell differentiation (39, 40). Chromo-
now be extinct. With these data, generation of a highly resolved
some numbers range from one to many hundreds, and some
eukaryotic tree of life will underpin analyses of the origins and
species have different chromosome complements in germline
diversification of genes in the core eukaryotic toolkit and in
and somatic nuclei through programmed DNA elimination (41,
organellar function.
42). Eukaryotes protect the ends of their chromosomes, the
telomeres, from unavoidable replication-associated erosion
through the addition of diverse kinds of nongenomically tem-
Tracking Genomic Changes in Symbiosis
Symbiosis is a signature of eukaryotic life, generating ecological plated DNA (43). Centromeric function assures correct segrega-
diversity and organismal complexity across eukaryotic lineages. tion of chromosome sets to daughter cells based on specific
Primary productivity on land is based on mutualistic symbioses sequence features or epigenetic signals (44). The partitioning of
between vascular plants and root-colonizing microorganisms genes on different chromosomes also offers opportunity and
(33). Insect trophic niches are defined by acquisitions of benefi- constraint in the evolution of gene regulatory networks. Within
cial microbial symbionts (34, 35). Mutualistic partners often del- many eukaryotic taxa both karyotypes and synteny are generally
egate responsibility for essential processes to one another, conserved (45), while in others rearrangement is rampant even
enforcing codependence even in the face of barriers imposed on short evolutionary timescales (46). Important questions about
by immune and antipredation systems (36). Species exist with a chromosomes that can be addressed with complete sampling
microbiome that aids in food digestion and other processes, of eukaryotic genomes include:
and the genomes of the microbiome may be of relevance to • What were the likely karyotypes, 3D organizations, and syn-
understanding host physiology. Not all symbioses are mutualis- teny relationships of genomes at all the ancestral nodes of the
tic, and nearly one-third of described eukaryotic species are par- eukaryotic tree?
asites (exploitative symbionts) (37). Parasites generate strong • How are chromosome numbers stabilized in the formation of
selection pressures on hosts and thus promote the maintenance a new species?
of sex and the evolution of innate and adaptive immunity. Rec- • What constraints do mitosis and meiosis put on chromosome
ognition of the ubiquity and fundamental ecological impact of number and organization?
symbioses is recent and largely stems from genomic data, which • Are chromosome rearrangements the cause of major transi-
have shed light on symbiont origins, genome streamlining, and tions and adaptations in eukaryotic evolution?
endosymbiotic transfer of genes to hosts (38). The big questions • How did telomeres evolve and what is the significance of dif-
on symbioses that can be answered with genomes of all species ferent telomere maintenance mechanisms?
include: • Does the kind of centromere (e.g., holocentric versus centro-
meric) condition genome evolution?
• Should hosts and their microbiomes be considered as hologe-
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• What constraints does karyotype place on the evolution of


nomic superorganisms?
gene regulatory networks?
• Are there common themes in the evolution of parasitic and
mutualistic symbiont genomes? By generating chromosome-scale genome assemblies across
• What are the range and diversity of mechanisms at the gene the eukaryotic tree of life the evolution of chromosome organi-
and molecular levels that enable symbioses? zation at all scales can be explicitly addressed, from analysis of
• How do symbioses that are beneficial but not obligatory conservation of local synteny to karyotypic evolution, and the
impact the evolution of both partners? dynamics of centromere and telomere repositioning. These
• How common is symbiotic gene transfer, and what legacies data could support the development of novel synthetic
have vanished symbionts contributed to current-day organis- genomes with engineered chromosomal stability and other
mal function? behaviors for biomedical and industrial applications.

4 of 9 j PNAS Blaxter et al.


https://doi.org/10.1073/pnas.2115636118 Why sequence all eukaryotes?
Revealing the Deep Logic of Eukaryotic Gene Regulation small sperm) evolved independently multiple times, and paren-
Every eukaryotic genome contains thousands of protein-coding tal investment in eggs or sperm has led to evolution of extreme
genes and each has regulatory elements and circuits that sex differences in morphology, life-history strategy, and behav-
orchestrate how and when those genes are used. Most of these ior. There is tremendous variety in the mechanisms determining
elements (47, 48), including noncoding transcripts (short and sex, ranging from single-locus drivers and differentiated sex
long), promoters, enhancers, insulators, and the 3D structure chromosomes through to epigenetic and environmental deter-
(49, 50) of the genome itself, can be distinguished from non- mination (64, 65). The heterotypic sex chromosomes are often
functional DNA because their sequences are evolutionarily con- rapidly evolving, and sex determination mechanisms are often
strained (51). Vice versa, regions with an accelerated rate of invaded by non-Mendelian elements (66). Sex determination
change in particular lineages may be linked to new evolutionary systems provide strong evidence for evolution in action, but
adaptations (52). For individual species, a reference genome must simultaneously ensure continuing function of the essential
makes it possible to assay regulation in tissues and cells by mea- processes of reproduction. Specific questions on the evolution
suring gene expression, mapping open chromatin, detecting of sexual systems that can be addressed by complete sequenc-
histone modification states, detecting transcription factor bind- ing of eukaryotic lineages include:
ing, and determining the 3D organization of chromatin against
• How often has a male–female system evolved independently,
the reference genome assembly (48, 53). Some regulatory net-
and how have systems with multiple mating types evolved
works evolve rapidly, while others are apparently strongly
and been maintained?
constrained (54). Using comparative genomics, functional anno-
• Do changes in the sex determination system drive speciation,
tations experimentally determined in one species can be
and how is this reflected in the genome?
mapped across to related species, providing a rapid, in-depth
• In species with segregated germlines (ciliates and most ani-
genome annotation of a whole clade (55). Specific questions
mals), how is the germline specified and how is the germline
that can be addressed include:
genome maintained?
• What is the comprehensive list of all eukaryotic genes? • How is chromatin diminution distributed across the tree of
• What are the building blocks of eukaryotic genome regula- life, and how is it regulated?
tion? How stable are they? • Are there viable alternatives to meiotic recombination (such
• How do new regulatory regimes arise and supplant existing as gene conversion) that would allow ancient asexuals to
systems? avoid Muller’s ratchet, or do ancient asexuals just have sex
• Can deep multispecies whole-genome alignments reveal new very rarely?
classes of conserved elements?
Reference genome sequences for all taxa would lay bare the
• What genomic features distinguish conserved regulatory
dynamics of the genomic causes and consequences of the evo-
networks?
lution of sex determination systems. With chromosomally com-
• How do regulatory networks constrain chromosome and
plete sequences, the dynamics of change in the sex-restricted
genome evolution?
chromosome in heterogametic groups could be precisely
The power to discern patterns of constraint and acceleration defined. Knowledge of the sexual systems of pests and para-
depends on the number of species compared, and how closely sites could be used to design gene drives that eliminate or
related they are. With genomes of all species, functional reduce populations.
sequences can be mapped with more sensitivity and at far
greater resolution (56, 57), and this functional variation can be Exploring Diversity in the Genomics of Speciation
connected to phenotypes (58). Only with high-quality genomes Although the reality of eukaryotic species is accepted, the pro-
can we map long-range chromosome interactions with confi- cess of speciation is still a matter of debate, and there are many
dence, and disentangle the effects of duplication, mobile element cases where species boundaries are leaky or incomplete. The
insertion, and repeat accumulation in modifying preexisting gene biological species concept posits stable reproductive isolation
regulation. It will be possible to map regulatory promoter regions between sister taxa (67, 68). However, genomic data show that
of protein-coding genes and long noncoding RNA, duplications, ongoing gene exchange via hybridization and introgression
repeats, and transposable element insertions that are a crucial after taxonomically accepted speciation is common, if not ubiq-
source of innovations of gene regulation (12, 59, 60). A far deeper uitous, and can occur over unexpectedly long time spans since
understanding of the regulatory genome, and how it functions, initial separation (69). Frequently, nominal species concepts
will be gained than would ever be possible if each species was hide multiple cryptic taxa, and many species have yet to be dis-
considered in isolation. covered and named. For these new taxa, genomic data may be
critical in discovery and definition (70). From the perspective of
Probing the Diversity of Sexual Systems genetics and genomics, species separation is a process, not an
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Sexual reproduction is a deep common thread in eukaryotes. It event. Even in the absence of hybridization, variation at some
likely evolved to permit efficient mixing of alleles at linked loci loci remains shared (incomplete lineage sorting) typically for
to colonize new niches and escape parasites and pathogens thousands to millions of generations even after total separation
(61). Asexual lineages are threatened by fitness degradation (20). The genetics and genomics of speciation mechanisms
through accumulation of deleterious mutations (Muller’s ratchet) range from single loci of large effect, through inversions that
and are short-lived in phylogenetic terms, and putatively ancient suppress recombination or generate Haldane’s rule effects on
asexuals appear to undergo rare sexual reproduction (62, 63). the heterogametic sex, to genomes that have fully diverged
Some protist groups, such as ciliates, have multiple equivalent in allopatry. Specific questions on speciation that can be
mating types, but most multicellular organisms have two sexes. addressed by complete sequencing of eukaryotic lineages
Production of differentiated haploid gametes (large eggs and include:

Blaxter et al. PNAS j 5 of 9


Why sequence all eukaryotes? https://doi.org/10.1073/pnas.2115636118
• How diverse are the processes of speciation and how do they • What genomic and genetic architectures produce plasticity in
pattern genomes? responses and thus resistance or malleability to environmental
• What genomic signals distinguish incomplete lineage sorting, change?
introgression, and hybridization?
As the wider program of the EBP is achieved, the number of
• Are certain kinds of genes and gene networks more likely to
informative, independent replications of traits of interest acces-
be implicated in speciation?
sible to whole-genome comparison will multiply, and these
• What roles does chromosome rearrangement play in
comparisons will be powerful because of the uniform quality of
speciation?
the genome assemblies and annotations. To achieve this vision,
• Do different reproductive strategies drive different genomic
existing large-scale, rich, and open trait databases will need to
structures that impact on speciation?
be enhanced, collating physiological, life-history, and anatomi-
• How do macroevolutionary phenomena such as species radia-
cal metadata that can be analyzed in the context of contiguous
tions pattern the genome?
chromosome-level genome assemblies. Whole-genome align-
• Is future speciation predictable from current-day genomes?
ment across many species can isolate trait loci to likely nucleo-
By sampling the full spectrum of species distinctiveness from tide, regulatory, and structural variants. Reference genomes for
ongoing hybridization to complete separation, the EBP will pro- all taxa will also open each and every species-variable trait of
vide an enormously rich dataset to address key questions about interest to high-throughput genetic analysis. Overall, this com-
the diverse processes of speciation and the impacts of specia- parative genomic approach, with high-quality genomes, applied
tion on genome structure and content. Genomics will become to thousands of specialized traits in thousands of species, will
part and parcel of species description. A complete set of lead to a new understanding of genotype–phenotype relation-
sequenced eukaryotic genomes will allow us to gain a deeper ships, and ultimately define the rules of life (26).
appreciation of not just the diversity of species but also the
diversity of speciation mechanisms. We will develop a much Understanding Ecosystem Function, Stasis, and Change
richer appreciation of the ways in which species are distinct Biological diversity is often quantified by numbers of species in
from each other. communities and in geographic regions, but ecological com-
plexity and functioning are driven by species interactions.
Organisms can be identified and counted using genetic signa-
Decoding the Genomics of Complex Traits
tures (DNA barcodes, environmental DNA), an approach limited
Deciphering the genetic basis of complex traits has been one of
only by the completeness of the reference libraries with which
the most challenging problems in contemporary biology, agri-
the signatures are compared (74). The biosynthetic capabilities
culture, and medicine. Variation in complex traits is generated
and metabolic dependencies of species determine their abiotic
by environmental, genetic, and genotype-by-environment inter-
ranges and thus potential species interactions, including coevo-
actions under the control of many genes with a range of effect
lutionary relationships (75). A combination of genomic and eco-
sizes (71). Genome-wide association studies using thousands of
logical data can more completely elucidate species interaction
single-nucleotide polymorphisms have confirmed the genetic
networks within natural and human-dominated ecosystems (76).
complexity of quantitative traits and in some cases identified
Because the interplay among species in a community is
the genes or regulatory elements responsible for the genetic
dynamic, adding historical dimensions to genomic investiga-
component of heritability estimates. However, the identity and
tions allows prediction of how ecosystems and species interac-
modes of action of loci underpinning most complex traits
tions will respond as environments undergo rapid change (77).
remain enigmatic, and the roles of epigenetic factors in regulat-
One current, major ecosystem challenge is the increasing intro-
ing complex traits have only recently come into focus. Compar-
duction of invasive species that can degrade local ecosystem
ative genomics across multiple independent origins can be
function. Complete identification of species in ecosystems,
used to identify convergent evolution of complex traits among
including bacteria and archaea, will allow several grand chal-
species (26). For example, vocal learning evolved independently
lenge questions to be addressed, including:
in several bird and mammal lineages, with convergent changes
in expression of several hundred genes implicated in human • What are the genomic signatures within and between species
speech (72), and repeated origins of sociality in bees are associ- that drive long-term interactions in biological communities
ated with changes in gene regulation (73). Sequenced genomes and ecosystems?
from across the eukaryotic tree of life can thus serve as a power- • What is the genomic basis of ecological resilience?
ful resource for addressing important questions about the geno- • Can damaged or lost ecosystems be restored using knowl-
mic architecture of complex traits, such as: edge of all species in the healthy state?
• Can invasiveness be predicted from species genomes, and
• What is the genomic nature of morphological homology?
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can we use genomics to mitigate the effects of these invasive


• What traits can be mapped with higher power across versus
species?
within species?
• Where traits are shared by disparate taxa, what are the rela- A digital library of eukaryotic life will provide an anchored
tive contributions of genetic homology (i.e., traits generated source of reference sequences for DNA barcoding, metage-
by homologous genetic toolkits) versus convergence? nomic, environmental DNA, and ancient DNA approaches to
• What genomic features predict and likely underpin the physio- large-scale, high-throughput monitoring, and biosurveillance of
logical systems that drive core traits of interest to conserva- present and past ecosystems. A library of all genomes will allow
tion, human health, agriculture, and bioprocessing? any environmentally sampled DNA sequence to be assigned to
• Can organismal responses to climate change or other environ- its species and even population of origin. Taxon presence and
mental disturbances be predicted from their genomes? abundance derived from sequence surveys can link to the

6 of 9 j PNAS Blaxter et al.


https://doi.org/10.1073/pnas.2115636118 Why sequence all eukaryotes?
physiology of species inferred from their genomes, and thus be error-free genome assemblies for eukaryotes (11) at scale (12),
transformed into assessments of ecosystem balance (78). Even and high-quality genome sequencing from single, small speci-
with the genome sequence of one individual, the coalescent his- mens is becoming possible (84). These genome references are
tory recorded in the genome can be used to estimate ancestral still estimates of the true genome sequence of an individual, but
population sizes and thus compare current interactions with those are orders of magnitude more contiguous and have higher per-
of past ecosystems. Genomic understanding will enhance under- base accuracy than previous generations of assemblies (11, 60).
standing of community species composition in time and space. Similarly, while the discovery of coding and other features in
genomes is still not perfect, current methodologies are generat-
Building Genomics-Informed Conservation ing very highly credible gene sets for downstream analyses. Turn-
Earth is currently experiencing a sixth mass extinction of spe- ing a genome into a functioning organism is still something only
cies, caused by humans (79). Species extinction is largely driven the machinery of a living cell can do, but tools for predicting phys-
by habitat loss, either directly through habitat destruction, iology and phenotypes from genome sequences are maturing
including fragmentation, or indirectly via climate change. Biodi- rapidly, and inference of function will be made more robust with
versity is critical for maintenance of the essential ecosystem more complete, high-quality genomes, enhancing our phenotypic
services on which human society depends (80, 81). While biodi- predictive power. The challenges include:
versity loss is a product of runaway anthropogenic degradation,
• Can we reliably and affordably generate telomere-to-telomere
our active conservation and expansion of biodiversity are also
assemblies for all species, even those that have very few cells
part of the solution to the climate crisis. At the single-species
or that have very large genomes (or both)?
level, there are concerns for the current, past, and dynamics of
• Can we generate highly accurate estimates of the transcrip-
change of the gene pools of species, and captive or directed
tionally active parts of a genome, and thus of the proteins
breeding initiatives rely on assessment and avoidance of
encoded and biochemical pathways present?
inbreeding. Ecosystem fragmentation isolates different taxa in
• Can the tools for comparative genomics (annotation, align-
different ways, and building back from degraded fragments
ment, orthology inference) be refactored to analyze hundreds
requires understanding of effects across diversity. These press-
to tens of thousands of genomes simultaneously?
ing issues raise questions for all of society, and reference-
quality genomes for all eukaryotes can be part of the answers. We are quietly but unashamedly optimistic in our assessment
of both the possibility and promise of the scale of genomics that
• How can ecosystem genomics be deployed to promote con-
is proposed. Sequencing strategies are being refined actively,
servation of unsurveyed diversity?
such that high-quality genome assemblies can be derived from
• Can genomics robustly infer extinction risk and routes to
even single small specimens and good draft-quality genomes
extinction prevention, or even deextinction, for diverse
from single cells (85). Algorithms that fully exploit the information
species?
contained in long-read sequence data are already reducing the
• Can predictions of extinction risk estimated from genome
computational costs of assembly while improving quality (86, 87).
sequencing be integrated across species in an ecosystem?
The annotation challenge is being met by new approaches, for
• Is conservation of nearly neutral genetic diversity as important
example by leveraging the comparison between multiple
as conservation of adaptively evolving loci?
genomes to identify conserved (and thus likely functional) regions
• How can genetic resilience be promoted in an ever-changing
(57, 88). The postgenome analytic processes are being conquered
world where adaptation is needed in a geologically very short
by rapid heuristic tools and the application of new data models,
time frame?
and will spur development of new statistical methodologies. In
Sequencing life is an opportunity to help preserve life. We the end, the EBP will only achieve its goals if our tools are up to
suggest that the sequencing of the genomes of all species will the task, and in building a toolkit that works at scale for the first
change how we understand and analyze their characteristics 100,000 genomes we will, we believe, deliver a toolkit that works
and interactions, their population structures, and their likely for millions. These tools will also serve the explosion of postge-
capacity to adapt to rapid ecological change (8). The genomes nomic research we expect to nurture and support.
of novel potential crops and crop relatives, and of diverse spe-
cies that synthesize novel bioactive compounds, can build a Conclusion and Outlook
new value economy where biodiversity is inherently valued for The availability of highly accurate and fully assembled and
its future potential in agriculture or medicine. Genomically annotated genomes densely sampled from across the millions
informed rewilding and ecosystem restoration could transform of species on Earth will transform biological understanding
our planet and promote human coexistence with a thriving natu- (Fig. 1). This library of all life will preserve for posterity the diver-
ral world. The skills built in rescuing our planet could be sity and history of this planet’s biology. The genomes will be
deployed in terraforming others. This knowledge will be key to the core data from which the phylogeny of all life is inferred,
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preservation of species and interventions that maintain balance including the complex reticulations that endosymbiosis, hori-
within ecosystems, and will drive effective, data-driven ecosys- zontal transfer, hybridization, and introgression have created.
tem conservation (82). Complete genome assemblies enable a broader and more com-
plete understanding of a species’ biology, contributing to a
Inventing New Tools and Resources lessened risk of extinction. Within the unifying model of this
Historically, genome sequencing and assembly have been skilled phylogenetic network, the genomes and the genes they pos-
labors, each polished genome the product of years of human sess will enable understanding of regulatory networks and trait
effort (83). This has to change, without compromising on quality. evolution, the dynamics of coevolution between genes and
While already routine for small bacterial and viral genomes, it is between species, the impact of changing environments on spe-
only now becoming possible to generate near-complete and cies and populations, the mechanistic link between genotypes

Blaxter et al. PNAS j 7 of 9


Why sequence all eukaryotes? https://doi.org/10.1073/pnas.2115636118
and phenotypes, and the drivers of genome–environment inter- Please Join the Conversation
actions. These analyses, in turn, will enable biologists to better The big questions we have posed derive from our collective
characterize fundamental evolutionary processes, from the discussions, but we are aware—and indeed hope—that
nucleotide to the genome level, identifying processes active there will be additional major questions that others believe
under different chromosomal architectures and gene interaction can be answered by sequencing and functionally annotating
networks. These dramatic advances in understanding of both all eukaryotic genomes. We invite you to add questions to
the wide sweep and the local details of genomic and organismal the roster, to widen the debate, and to, ultimately, fully real-
evolution will enable the inference of ancestral genomes and ize the promise of biological understanding based on the
their traits, which will be transformative for understanding how complete genome sequence of all of Earth’s remarkable
life evolved on Earth, predicting future evolution, and inspiring species.
bioengineering of organisms with beneficial traits using technol-
ogies such as CRISPR and whole-genome synthesis. This foun- Data Availability. There are no data underlying this work.
dational library of information will change the economic and
social growth of the future, fostering sustainable agriculture and Acknowledgments
This research was funded in whole, or in part, by Wellcome Trust Grants 206194
new bioeconomies, accessing an expanded medical pharmaco-
and 218328. For the purpose of open access, we have applied a CC BY public
poeia, and promoting societal equity and diversity through the copyright license to any author-accepted manuscript version arising from this
lens of a deeply valued biodiversity. submission.

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Why sequence all eukaryotes? https://doi.org/10.1073/pnas.2115636118

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