The others: our biased perspective of eukaryotic genomes

•There is an important bias in eukaryotic knowledge, affecting cultures and genomes.•Eukaryotic genomics are biased towards multicellular organisms and their parasites.•A phylogeny-driven initiative is needed to overcome the eukaryotic genomic bias.•We propose to sequence neglected cultures and increase culturing efforts.•Single-cell genomics should be embraced as a tool to explore eukaryotic diversity. Understanding the origin and evolution of the eukaryotic cell and the full diversity of eukaryotes is relevant to many biological disciplines. However, our current understanding of eukaryotic genomes is extremely biased, leading to a skewed view of eukaryotic biology. We argue that a phylogeny-driven initiative to cover the full eukaryotic diversity is needed to overcome this bias. We encourage the community: (i) to sequence a representative of the neglected groups available at public culture collections, (ii) to increase our culturing efforts, and (iii) to embrace single cell genomics to access organisms refractory to propagation in culture. We hope that the community will welcome this proposal, explore the approaches suggested, and join efforts to sequence the full diversity of eukaryotes. Understanding the origin and evolution of the eukaryotic cell and the full diversity of eukaryotes is relevant to many biological disciplines. However, our current understanding of eukaryotic genomes is extremely biased, leading to a skewed view of eukaryotic biology. We argue that a phylogeny-driven initiative to cover the full eukaryotic diversity is needed to overcome this bias. We encourage the community: (i) to sequence a representative of the neglected groups available at public culture collections, (ii) to increase our culturing efforts, and (iii) to embrace single cell genomics to access organisms refractory to propagation in culture. We hope that the community will welcome this proposal, explore the approaches suggested, and join efforts to sequence the full diversity of eukaryotes. Eukaryotes are the most complex of the three domains of life. The origin of eukaryotic cells and their complexity remains one of the longest-debated questions in biology, famously referred to by Roger Stanier as the ‘greatest single evolutionary discontinuity’ in life [1Stanier R.Y. et al.The Microbial World. Prentice-Hall, 1957Google Scholar]. Thus, understanding how this complex cell originated and how it evolved into the diversity of forms we see today is relevant to all biological disciplines including cell biology, evolutionary biology, ecology, genetics, and biomedical research. Progress in this area relies heavily on both genome data from extant organisms and on an understanding of their phylogenetic relationships. Genome sequencing is a powerful tool that helps us to understand the complexity of eukaryotes and their evolutionary history. However, there is a significant bias in eukaryotic genomics that impoverishes our understanding of the diversity of eukaryotes, and leads to skewed views of what eukaryotes even are, as well as their role in the environment. This bias is simple and widely recognized: most genomics focuses on multicellular eukaryotes and their parasites. The problem is not exclusive to eukaryotes. The launching of the so-called ‘Genomic Encyclopedia of Bacteria and Archaea’ [2Wu D. et al.A phylogeny-driven genomic encyclopaedia of Bacteria and Archaea.Nature. 2009; 462: 1056-1060Crossref PubMed Scopus (769) Google Scholar] has begun to reverse a similar bias within prokaryotes, but there is currently no equivalent for eukaryotes. Targeted efforts have recently been initiated to increase the breadth of our genomic knowledge for several specific eukaryotic groups, but again these tend to focus on animals [3Pennisi E. No genome left behind.Science. 2009; 326: 794-795Crossref PubMed Scopus (8) Google Scholar], plants [4Bennetzen J. Kellogg E. A plant genome initiative.Plant Cell. 1998; 10: 488-494Crossref Scopus (9) Google Scholar], fungi [5Galagan J.E. et al.Genomics of the fungal kingdom: insights into eukaryotic biology.Genome Res. 2005; 15: 1620-1631Crossref PubMed Scopus (227) Google Scholar], their parasites [6Degrave W.M. et al.Parasite genome initiatives.Int. J. Parasitol. 2001; 31: 532-536Crossref PubMed Scopus (34) Google Scholar], or opisthokont relatives of animals and fungi [7Ruiz-Trillo I. et al.A phylogenomic investigation into the origin of metazoa.Mol. Biol. Evol. 2008; 25: 664-672Crossref PubMed Scopus (182) Google Scholar]. Unfortunately, a phylogeny-driven initiative to sequence eukaryotic genomes specifically to cover the breadth of their diversity is lacking. The tools already exist to overcome these biases and fill in the eukaryotic tree, and we therefore hope that researchers will be inspired to explore these tools and embrace the prospect of working towards a community-driven initiative to sequence the full diversity of eukaryotes. It is not surprising that the first and main bias in the study of eukaryotes arises from our anthropocentric view of life. More than 96% of the described eukaryotic species are either Metazoa (animals), Fungi, or Embryophyta (land plants) [8Pawlowski J. et al.CBOL Protist Working Group, barcoding eukaryotic richness beyond the Animal, Plant, and Fungal Kingdoms.PLoS Biol. 2012; 10: e1001419Crossref PubMed Scopus (374) Google Scholar] (Figure 1A) – which we call the ‘big three’ of multicellular organisms (even though the Fungi also include unicellular members such as the yeasts). However, these lineages only represent 62% of the 18S rDNA (see Glossary) Genbank sequences (Figure 1B), which is of course a biased sample, or 23% of all operational taxonomic units (OTUs) in environmental surveys (Figure 1C). This bias is not new; research has historically focused on these three paradigmatic eukaryotic kingdoms, which are indeed important, but are also simply more conspicuous and familiar to us. In genomics this bias is amplified considerably: 85% of the completed or projected genome projects {as shown by the Genomes OnLine Database (GOLD) [9Pagani I. et al.The Genomes OnLine Database (GOLD) v.4, status of genomic and metagenomic projects and their associated metadata.Nucleic Acids Res. 2012; 40: D571-D579Crossref PubMed Scopus (370) Google Scholar]} belong to the ‘big three’ (Figure 1D). Moreover, even within these groups there are biases. For example, many diverse invertebrate groups suffer from a lack of genomic data as keenly as do microbial groups. This makes for a pitiful future if we aim to understand and appreciate the complete eukaryotic tree of life. If we do not change this trend we risk neglecting the majority of eukaryotic diversity in future genomic or metagenomic-based ecological and evolutionary studies. This would provide us with a far from realistic picture. The ‘multicellular bias’ is the most serious, but is not alone. The eukaryotic groups with most species deposited in culture collections and/or genome projects are also biased towards either those containing mainly phototrophic species or those that are parasitic and/or economically important (Figure 2). For example, both Archaeplastida and Stramenopila have more cultured species than other eukaryotes as a result of a long phycological tradition and the well-provided phycological culture collections [10Day J.G. et al.Pringsheim's living legacy: CCALA, CCAP, SAG and UTEX culture collections of algae.Nova Hedwigia. 2004; 79: 27-37Crossref Scopus (17) Google Scholar], and also because they are easier to maintain in culture than heterotrophs. In both cases this translates to a comparatively large number of genome projects: several genomic studies target photosynthetic stramenopiles [11Bowler C. et al.The Phaeodactylum genome reveals the evolutionary history of diatom genomes.Nature. 2008; 456: 239-244Crossref PubMed Scopus (1202) Google Scholar, 12Cock J.M. et al.The Ectocarpus genome and the independent evolution of multicellularity in brown algae.Nature. 2010; 465: 617-621Crossref PubMed Scopus (620) Google Scholar] and, owing to their economic relevance in the agriculture, the peronosporomycetes [13Pais M. et al.From pathogen genomes to host plant processes: the power of plant parasitic oomycetes.Genome Biol. 2013; 14: 211Crossref PubMed Scopus (48) Google Scholar]. In addition, the apicomplexans within the Alveolata are also relatively well studied at the genomic level because they contain important human and animal parasites [14Van Dooren G.G. Striepen B. The algal past and parasite present of the apicoplast.Annu. Rev. Microbiol. 2013; 67: 271-289Crossref PubMed Scopus (107) Google Scholar] such as Plasmodium and Toxoplasma. If we look instead at the number of sequenced strains rather than species, these biases are increased further (Figure 3). As a result, a significant proportion of the retrieved cultures and genomes correspond to different strains of the same we have a of species that have been cultured and diversity the The with the most strains in the culture The with the most genome The most in the operational taxonomic sequence single amplified full strains are not described at the species level and have been by they represent more than a single strains are not described at the species level and have been by they represent more than a single we lack an phylogenetic tree of the eukaryotes, a tree is to D. et for the tree of Biol. PubMed Scopus Google Scholar]. The of eukaryotes are in The of cultured and sequenced species the tree a of our current knowledge of eukaryotic diversity (Figure However, a of the lineages lack even a single culture in of the culture collections and, of lack a The most important are within the the and the many lineages are However, many other lineages that lack representative genome sequence are also in the relatively and groups. This is to be because several genome projects not be in the and because many cultures are not deposited in culture collections, but the an of the biases we currently eukaryotic to to and to the efforts of many we have in our understanding of the tree of eukaryotes. to the most et al.The of Microbiol. 2012; PubMed Scopus Google Scholar], the eukaryotes be into We these specific of this of most of a relatively simple life and as well as a organisms et and of the 2005; PubMed Scopus Google Scholar]. are and include the of and a in the study of the origin of also as or this the and the The Archaeplastida is one of the groups of photosynthetic eukaryotes et and evolution of the Rev. 2012; 31: Scopus Google Scholar]. are diverse and in The plants are the most on and plants have historically a role in the the of The of with to the J. Scopus Google Scholar], and phylogenomic et the of and eukaryotic 2009; PubMed Scopus Google Scholar]. members of this are human parasites such as of and of as well as animal parasites such as of as well as and of and the include of the of the Metazoa and the phylogenetic and phylogenomic have shown that the also include several unicellular lineages et within the on phylogenomic of single Biol. Evol. PubMed Scopus Google Scholar]. include the unicellular relatives of the and the include several parasites that on and three groups that have been historically studied have shown that those three groups a a as et the eukaryotic PubMed Scopus Google Scholar]. This eukaryotic the diversity within the also as the stramenopiles include a of phototrophic and organisms I. et of 2009; PubMed Scopus Google Scholar]. are unicellular but there are also multicellular such as the relevant members of the Stramenopila are the within a cell the in the groups most microbial of the and plant parasites such as the a of unicellular eukaryotes that have diverse life such as and et evolution Microbiol. PubMed Scopus Google Scholar]. include relevant groups such as the the and the as well as the that parasites such as Plasmodium of of and this is a diverse of unicellular eukaryotes including both and forms Biol. PubMed Scopus Google Scholar]. groups, and the are members of the have been in and to their that be in the for a to those organisms or lineages with to to and to the efforts of many we have in our understanding of the tree of eukaryotes. to the most et al.The of Microbiol. 2012; PubMed Scopus Google Scholar], the eukaryotes be into We these specific of this of most of a relatively simple life and as well as a organisms et and of the 2005; PubMed Scopus Google Scholar]. are and include the of and a in the study of the origin of also as or this the and the The Archaeplastida is one of the groups of photosynthetic eukaryotes et and evolution of the Rev. 2012; 31: Scopus Google Scholar]. are diverse and in The plants are the most on and plants have historically a role in the the of The of with to the J. Scopus Google Scholar], and phylogenomic et the of and eukaryotic 2009; PubMed Scopus Google Scholar]. members of this are human parasites such as of and of as well as animal parasites such as of as well as and of and the include of the of the Metazoa and the phylogenetic and phylogenomic have shown that the also include several unicellular lineages et within the on phylogenomic of single Biol. Evol. PubMed Scopus Google Scholar]. include the unicellular relatives of the and the include several parasites that on and three groups that have been historically studied have shown that those three groups a a as et the eukaryotic PubMed Scopus Google Scholar]. This eukaryotic the diversity within the also as the stramenopiles include a of phototrophic and organisms I. et of 2009; PubMed Scopus Google Scholar]. are unicellular but there are also multicellular such as the relevant members of the Stramenopila are the within a cell the in the groups most microbial of the and plant parasites such as the a of unicellular eukaryotes that have diverse life such as and et evolution Microbiol. PubMed Scopus Google Scholar]. include relevant groups such as the the and the as well as the that parasites such as Plasmodium of of and this is a diverse of unicellular eukaryotes including both and forms Biol. PubMed Scopus Google Scholar]. groups, and the are members of the have been in and to their that be in the for a to those organisms or lineages with there not be organisms for genome there are if we aim to understand eukaryotic diversity. We argue that at of the should be specifically towards the in the eukaryotic tree of on those lineages that phylogenetic that be is to sequence more cultured In of species in culture are not for a genome (Figure in the data Thus, by the genome of available cultured lineages that have not been we fill of the important of the tree, including and However, species that are available in culture is and most lineages cultured representative J. et bias in 2013; PubMed Scopus Google Scholar]. collections as the and the of and in are than their or fungal the is the lack of a of described in to the for et of of Scholar]. and of the species with genome projects completed or in are not deposited in of the culture more in the future the community should and similar to those in to cultures to The community will from this in the and long In addition, there is an bias in as well as a bias in culturing For example, phototrophic of Stramenopila and Alveolata tend to have more cultures available than their (Figure of the most strains present in culture collections are phototrophic organisms (Figure 3). there is a both to increase the culturing for a of and to and culture to refractory organisms J. et the of the J. 2013; PubMed Scopus Google Scholar], both of which and culture collections will to be that they on the of more cultures and their to include more organisms that tend to be from collections, in culture collections are for the of all disciplines. are to the of organisms and, to a understanding of their biology. we of the a biological in with the aim of a to to all the collections include a of biological such as cell genomics and The more than strains of different of and fungal and strains of of and a culture by the that and from both and The of by and and the cultures they at the of the of in the to the and by in In these cultures the of the of and that the for and this of and a and by the in The originated from culture collections by at and at it in the it as the of and to the community algal cultures of or for this is at the and is to the of this maintain more than strains of and from of the strains are available for are in the of of at the SAG is a by the of The and from or but there are also more than the SAG is the three culture collections of in the is also the of the it initiated in to as a in on the algal has been and into the we collections are for the of all disciplines. are to the of organisms and, to a understanding of their biology. we of the a biological in with the aim of a to to all the collections include a of biological such as cell genomics and The more than strains of different of and fungal and strains of of and a culture by the that and from both and The of by and and the cultures they at the of the of in the to the and by in In these cultures the of the of and that the for and this of and a and by the in The originated from culture collections by at and at it in the it as the of and to the community algal cultures of or for this is at the and is to the of this maintain more than strains of and from of the strains are available for are in the of SAG of at the SAG is a by the of The and from or but there are also more than the SAG is the three culture collections of in the is also the of the it initiated in to as a in on the algal has been and into the we A to increase the breadth of eukaryotic genomics is to single cell genomics et genomics reveals in PubMed Scopus Google Scholar]. the is this is the we have today to genomic from microbial eukaryotes that are relevant but are refractory to For example, the single amplified genomes from different the fill well the culture and genomic that of the most groups in the suffer from (Figure In a significant of the correspond to organisms such as the stramenopiles and et the majority in the of within J. 2013; PubMed Scopus Google Scholar], groups and J. diversity within and on PubMed Scopus Google Scholar], and the et and diversity of to Microbiol. 2008; 10: PubMed Scopus Google Scholar]. sequence that only of the are present in culture and only have an genome on cultured It is that the far available represent only Thus, the overcome of the they do not cover the full diversity of eukaryotes. the of to further our understanding of eukaryotic an important to is genome data be from et genomics reveals in PubMed Scopus Google Scholar]. there to be a diversity of owing to the bias by the The of the retrieved genome from than to a complete and on the of the cell studied as well as on the cell an look at Microbiol. 2012; 15: PubMed Scopus Google Scholar]. a more to a genome of at and a species in culture also researchers with a to the of the and research. and even all be in a for the genome and the However, in of the lack of data we currently and the that a significant increase in for will we argue that genomic sequencing of is an important to research in our understanding of eukaryotic diversity. Genome sequences have on the of in many cases species 3). However, the available genome sequences of eukaryotes do not us only the of the also significant to our understanding of eukaryotic in and to evolutionary and ecological for this to be we and there are currently important in the diversity of eukaryotic genome sequences that our efforts to on this Understanding the of eukaryotic diversity will to our understanding of specific biological including of our more in agriculture, and of and our understanding of eukaryotic understanding on the eukaryotic diversity has a in several biological disciplines such as agriculture, and A large of research this we a that the power of a understanding of the biology, and evolution of has from evolutionary studies in eukaryotes. on the genome and of relatives of parasites have insights into in the of parasites. A taxonomic of organisms has also been the to A is an pathogen affecting for to a of taxonomic It not data researchers to to the in that on be et sequence to be a of the PubMed Scopus Google Scholar]. The with the the of the data that are peronosporomycetes within the and not fungi as the of M. and future Biol. 2010; PubMed Scopus Google Scholar]. knowledge of genome insights not only into evolution but also into the for to forms et sequence and of the pathogen 2009; PubMed Scopus Google in evolutionary studies the of a of eukaryotes is more and in it is that the of in evolutionary to that are to be in The is that to which genomic or have been which to eukaryotes, and which are one to that include from eukaryotic For of in and Fungi, and the of representative from and to the of the unicellular of et origin of the and 2010; PubMed Scopus Google Scholar] and the eukaryotic et and of a genome Biol. Evol. Scopus Google Scholar], is also by a understanding of biology. The ecological are by several groups of eukaryotes, most of We have a understanding of phototrophic eukaryotes with the most of the and the on our understanding of remains For example, both and the are extremely in the et insights into the diversity of 2009; Scopus Google Scholar]. they are in However, we understand their role if we lack on their or biology, we only from genomic A understanding on the eukaryotic diversity has a in several biological disciplines such as agriculture, and A large of research this we a that the power of a understanding of the biology, and evolution of eukaryotes. has from evolutionary studies in eukaryotes. on the genome and of relatives of parasites have insights into in the of parasites. A taxonomic of organisms has also been the to A is an pathogen affecting for to a of taxonomic It not data researchers to to the in that on be et sequence to be a of the PubMed Scopus Google Scholar]. The with the the of the data that are peronosporomycetes within the and not fungi as the of M. and future Biol. 2010; PubMed Scopus Google Scholar]. knowledge of genome insights not only into evolution but also into the for to forms et sequence and of the pathogen 2009; PubMed Scopus Google Scholar]. It in evolutionary studies the of a of eukaryotes is more and in it is that the of in evolutionary to that are to be in The is that to which genomic or have been which to eukaryotes, and which are one to that include from eukaryotic For of in and Fungi, and the of representative from and to the of the unicellular of et origin of the and 2010; PubMed Scopus Google Scholar] and the eukaryotic et and of a genome Biol. Evol. Scopus Google Scholar], is also by a understanding of biology. The ecological are by several groups of eukaryotes, most of We have a understanding of phototrophic eukaryotes with the most of the and the on our understanding of remains For example, both and the are extremely in the et insights into the diversity of 2009; Scopus Google Scholar]. they are in However, we understand their role if we lack on their or biology, we only from genomic We propose that in the eukaryotic tree at the genomic level on phylogenetic diversity should be a for the We also argue that this be by a of three at one genome from lineages from which cultures are available should be This is a culture and genomic sequencing to efforts and to the target and sequencing efforts to culture diverse organisms should be by of the to include more species and by this but in researchers they that such is a efforts are and have a that makes and therefore will be in that and research the of such of the microbial and genomic should embrace the of and to the which we will be the to in of the tree in the all these efforts, should also the of community such as culture collections and the of that are to We that the is to reverse the genome sequencing bias in the tree of eukaryotes. We have in our all the needed to change this skewed view and further our understanding of eukaryotic and that to change is the will and a Thus, we hope that the eukaryotic community will welcome this to a representative and diverse ‘Genomic Encyclopedia of and to this with with with the of the are in all eukaryotes in many are also and and of these 18S rDNA has been as a to and eukaryotes at the species or level It is also the most widely eukaryotic phylogenetic cultured microbial strains do not and are the members of the from which they This bias and The culturing bias be the result of a lack of culturing efforts, or and/or culturing – or for species in the be refractory to and an for access to genome and sequencing and their associated an operational of a species or of In microbial ecology, and in ecology, this operational is in a of the 18S rDNA to a of sequences with that are to represent a single taxonomic the of single cell that be further in similar to from a to and sequence the genome of a single The of an that with the and of environmental by and from This is by sequencing of the is a powerful to and environmental approaches cell an look at Microbiol. 2012; 15: PubMed Scopus Google Scholar].

Récupéré en direct depuis OpenAlex et désinversé. Les résumés ne sont pas conservés dans cette base de données : les index inversés représentent 8,6 Go des 9,3 Go de texte de la base, et le serveur dispose de 13 Go libres.