The others: our biased perspective of eukaryotic genomes
2014; Elsevier BV; Volume: 29; Issue: 5 Linguagem: Inglês
10.1016/j.tree.2014.03.006
ISSN1872-8383
AutoresJavier del Campo, Michael E. Sieracki, Robert E. Molestina, Patrick J. Keeling, Ramón Massana, Iñaki Ruiz‐Trillo,
Tópico(s)Genomics and Phylogenetic Studies
Resumo•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 dominant species. Therefore, we have a pool of species that have been redundantly cultured and sequenced.Figure 3Eukaryotic diversity distribution among the analyzed databases. (A) The 25 speciesa with the most strains represented in the analyzed culture collections. (B) The 25 speciesa with the most ongoing genome projects. (C) The 25 most abundant SAGs OTU97 in the analyzed dataset. Abbreviations: MAST, marine stramenopile; OTU97, operational taxonomic unit (>97% sequence identity); SAG, single amplified genome.Show full captionaSome strains are not described at the species level and have been grouped by genus. Therefore they may represent more than a single species.View Large Image Figure ViewerDownload (PPT) aSome strains are not described at the species level and have been grouped by genus. Therefore they may represent more than a single species. Although we lack an incontrovertible, detailed phylogenetic tree of the eukaryotes, a consensus tree is emerging thanks to molecular phylogenies [15He D. et al.An alternative root for the eukaryote tree of life.Curr. Biol. 2014; 24: 465-470Abstract Full Text Full Text PDF PubMed Scopus (157) Google Scholar]. The five monophyletic supergroups of eukaryotes are summarized in Box 1. The distribution of cultured and sequenced species over the tree provides a broad overview of our current knowledge of eukaryotic diversity (Figure 4). However, a quarter of the represented lineages lack even a single culture in any of the analyzed culture collections and, notably, 51% of them lack a genome. The most important gaps are within the Rhizaria, the Amoebozoa, and the Stramenopila, where many lineages are still underrepresented. However, many other lineages that lack any representative genome sequence are also found in the relatively well-described Opisthokonta and Excavata groups. This map is likely to be incomplete because several genome projects may not be reflected in the GOLD database, and because many cultures are not deposited in culture collections, but the overall trends probably afford an accurate representation of the biases we currently face.Box 1The five eukaryotic supergroupsThanks to molecular phylogenetics, to ultrastructural analyses, and to the efforts of many researchers, we have in recent years advanced significantly our understanding of the tree of eukaryotes. According to the most recent consensus taxonomy [28Adl S.M. et al.The revised classification of eukaryotes.J. Eukaryot. Microbiol. 2012; 59: 429-514Crossref PubMed Scopus (1155) Google Scholar], the eukaryotes can be divided into five monophyletic supergroups. We here introduce these supergroups, detailing some specific features of each.Amoebozoa: this group consists of amoeboid organisms, most of them possessing a relatively simple life cycle and limited morphological features, as well as a few flagellated organisms [30Smirnov A. et al.Molecular phylogeny and classification of the lobose amoebae.Protist. 2005; 156: 129-142Crossref PubMed Scopus (101) Google Scholar]. They are common free-living protists inhabiting marine, freshwater, and terrestrial environments. Some well-known amoebozoans include the causative agent of amoebiasis (Entamoeba histolytica) and Dictyostelium sp., a model organism used in the study of the origin of multicellularity.Archaeplastida: also known as 'the green lineage' or Viridiplantae, this group comprises the green algae and the land plants. The Archaeplastida is one of the major groups of oxygenic photosynthetic eukaryotes [31Leliaert F. et al.Phylogeny and molecular evolution of the green algae.CRC Crit. Rev. Plant Sci. 2012; 31: 1-46Crossref Scopus (588) Google Scholar]. Green algae are diverse and ubiquitous in aquatic habitats. The land plants are probably the most dominant primary producers on terrestrial ecosystems. Both green algae and land plants have historically played a central role in the global ecosystem.Excavata: the group Excavata was proposed based of shared morphological characters [32Simpson A.G.B. Patterson D.J. The ultrastructure of Carpediemonas membranifera (Eukaryota) with reference to the 'Excavate hypothesis'.Eur. J. Protistol. 1999; 35: 353-370Crossref Scopus (93) Google Scholar], and was later confirmed through phylogenomic analyses [33Hampl V. et al.Phylogenomic analyses support the monophyly of Excavata and resolve relationships among eukaryotic 'supergroups'.Proc. Natl. Acad. Sci. U.S.A. 2009; 106: 3859-3864Crossref PubMed Scopus (373) Google Scholar]. Most members of this group are heterotrophic organisms, among them some well-known human parasites such as Trichomonas vaginalis (the agent of trichomoniasis) and Giardia lamblia (the agent of giardiasis), as well as animal parasites such as Leishmania sp. (the agent of leishmaniasis) as well as Trypanosoma brucei, and Trypanosoma cruzi (the agents of sleeping sickness and Chagas disease respectively).Opisthokonta: the opisthokonts include two of the best-studied kingdoms of life: the Metazoa (animals) and the Fungi. Recent phylogenetic and phylogenomic analyses have shown that the Opisthokonta also include several unicellular lineages [34Torruella G. et al.Phylogenetic relationships within the Opisthokonta based on phylogenomic analyses of conserved single copy protein domains.Mol. Biol. Evol. 2011; 29: 531-544Crossref PubMed Scopus (125) Google Scholar]. These include the Choanoflagellata (the closest unicellular relatives of the animals) and the Ichthyospora (that include several fish parasites that impact negatively on aquaculture).SAR (Stramenopila - Alveolata, and Rhizaria): three groups that have been historically studied separately. Phylogenetic analyses, however, have shown that those three groups share a common ancestor, forming a supergroup known as SAR [36Burki F. et al.Phylogenomics reshuffles the eukaryotic supergroups.PLoS ONE. 2007; 2: 790Crossref PubMed Scopus (297) Google Scholar]. This eukaryotic assemblage comprises the highest diversity within the protists.Stramenopila: also known as heterokonts, the stramenopiles include a wide range of ubiquitous phototrophic and heterotrophic organisms [37Riisberg I. et al.Seven gene phylogeny of heterokonts.Protist. 2009; 160: 191-204Crossref PubMed Scopus (91) Google Scholar]. Most are unicellular flagellates but there are also some multicellular organisms, such as the giant kelps. Other relevant members of the Stramenopila are the diatoms (algae contained within a silica cell wall), the chrysophytes (abundant in freshwater environments), the MAST (marine stramenopile) groups (the most abundant microbial predators of the ocean), and plant parasites such as the Peronosporomycetes.Alveolata: a widespread group of unicellular eukaryotes that have adopted diverse life strategies such as predation, photoautotrophy, and intracellular parasitism [29Fast N.M. et al.Re-examining alveolate evolution using multiple protein molecular phylogenies.J. Eukaryot. Microbiol. 2002; 49: 30-37Crossref PubMed Scopus (130) Google Scholar]. They include some environmentally relevant groups such as the Syndiniales, the Dinoflagellata, and the ciliates (Ciliophora), as well as the Apicomplexa group that contains notorious parasites such as Plasmodium sp. (the agent of malaria), Toxoplasma sp. (the agent of toxoplasmosis), and Cryptosporidium sp.Rhizaria: this is a diverse group of mostly heterotrophic unicellular eukaryotes including both amoeboid and flagellate forms [35Burki F. Keeling P.J. Rhizaria.Curr. Biol. 2014; 24: 103-107Abstract Full Text Full Text PDF PubMed Scopus (63) Google Scholar]. Two iconic protist groups, Haeckel's Radiolaria and the Foraminifera, are members of the Rhizaria. Foraminifera have been very useful in paleoclimatology and paleoceanography due to their external shell that can be detected in the fossil record.Incertae sedis: Latin for 'of uncertain placement', a term used to indicate those organisms or lineages with unclear taxonomical position. Thanks to molecular phylogenetics, to ultrastructural analyses, and to the efforts of many researchers, we have in recent years advanced significantly our understanding of the tree of eukaryotes. According to the most recent consensus taxonomy [28Adl S.M. et al.The revised classification of eukaryotes.J. Eukaryot. Microbiol. 2012; 59: 429-514Crossref PubMed Scopus (1155) Google Scholar], the eukaryotes can be divided into five monophyletic supergroups. We here introduce these supergroups, detailing some specific features of each. Amoebozoa: this group consists of amoeboid organisms, most of them possessing a relatively simple life cycle and limited morphological features, as well as a few flagellated organisms [30Smirnov A. et al.Molecular phylogeny and classification of the lobose amoebae.Protist. 2005; 156: 129-142Crossref PubMed Scopus (101) Google Scholar]. They are common free-living protists inhabiting marine, freshwater, and terrestrial environments. Some well-known amoebozoans include the causative agent of amoebiasis (Entamoeba histolytica) and Dictyostelium sp., a model organism used in the study of the origin of multicellularity. Archaeplastida: also known as 'the green lineage' or Viridiplantae, this group comprises the green algae and the land plants. The Archaeplastida is one of the major groups of oxygenic photosynthetic eukaryotes [31Leliaert F. et al.Phylogeny and molecular evolution of the green algae.CRC Crit. Rev. Plant Sci. 2012; 31: 1-46Crossref Scopus (588) Google Scholar]. Green algae are diverse and ubiquitous in aquatic habitats. The land plants are probably the most dominant primary producers on terrestrial ecosystems. Both green algae and land plants have historically played a central role in the global ecosystem. Excavata: the group Excavata was proposed based of shared morphological characters [32Simpson A.G.B. Patterson D.J. The ultrastructure of Carpediemonas membranifera (Eukaryota) with reference to the 'Excavate hypothesis'.Eur. J. Protistol. 1999; 35: 353-370Crossref Scopus (93) Google Scholar], and was later confirmed through phylogenomic analyses [33Hampl V. et al.Phylogenomic analyses support the monophyly of Excavata and resolve relationships among eukaryotic 'supergroups'.Proc. Natl. Acad. Sci. U.S.A. 2009; 106: 3859-3864Crossref PubMed Scopus (373) Google Scholar]. Most members of this group are heterotrophic organisms, among them some well-known human parasites such as Trichomonas vaginalis (the agent of trichomoniasis) and Giardia lamblia (the agent of giardiasis), as well as animal parasites such as Leishmania sp. (the agent of leishmaniasis) as well as Trypanosoma brucei, and Trypanosoma cruzi (the agents of sleeping sickness and Chagas disease respectively). Opisthokonta: the opisthokonts include two of the best-studied kingdoms of life: the Metazoa (animals) and the Fungi. Recent phylogenetic and phylogenomic analyses have shown that the Opisthokonta also include several unicellular lineages [34Torruella G. et al.Phylogenetic relationships within the Opisthokonta based on phylogenomic analyses of conserved single copy protein domains.Mol. Biol. Evol. 2011; 29: 531-544Crossref PubMed Scopus (125) Google Scholar]. These include the Choanoflagellata (the closest unicellular relatives of the animals) and the Ichthyospora (that include several fish parasites that impact negatively on aquaculture). SAR (Stramenopila - Alveolata, and Rhizaria): three groups that have been historically studied separately. Phylogenetic analyses, however, have shown that those three groups share a common ancestor, forming a supergroup known as SAR [36Burki F. et al.Phylogenomics reshuffles the eukaryotic supergroups.PLoS ONE. 2007; 2: 790Crossref PubMed Scopus (297) Google Scholar]. This eukaryotic assemblage comprises the highest diversity within the protists. Stramenopila: also known as heterokonts, the stramenopiles include a wide range of ubiquitous phototrophic and heterotrophic organisms [37Riisberg I. et al.Seven gene phylogeny of heterokonts.Protist. 2009; 160: 191-204Crossref PubMed Scopus (91) Google Scholar]. Most are unicellular flagellates but there are also some multicellular organisms, such as the giant kelps. Other relevant members of the Stramenopila are the diatoms (algae contained within a silica cell wall), the chrysophytes (abundant in freshwater environments), the MAST (marine stramenopile) groups (the most abundant microbial predators of the ocean), and plant parasites such as the Peronosporomycetes. Alveolata: a widespread group of unicellular eukaryotes that have adopted diverse life strategies such as predation, photoautotrophy, and intracellular parasitism [29Fast N.M. et al.Re-examining alveolate evolution using multiple protein molecular phylogenies.J. Eukaryot. Microbiol. 2002; 49: 30-37Crossref PubMed Scopus (130) Google Scholar]. They include some environmentally relevant groups such as the Syndiniales, the Dinoflagellata, and the ciliates (Ciliophora), as well as the Apicomplexa group that contains notorious parasites such as Plasmodium sp. (the agent of malaria), Toxoplasma sp. (the agent of toxoplasmosis), and Cryptosporidium sp. Rhizaria: this is a diverse group of mostly heterotrophic unicellular eukaryotes including both amoeboid and flagellate forms [35Burki F. Keeling P.J. Rhizaria.Curr. Biol. 2014; 24: 103-107Abstract Full Text Full Text PDF PubMed Scopus (63) Google Scholar]. Two iconic protist groups, Haeckel's Radiolaria and the Foraminifera, are members of the Rhizaria. Foraminifera have been very useful in paleoclimatology and paleoceanography due to their external shell that can be detected in the fossil record. Incertae sedis: Latin for 'of uncertain placement', a term used to indicate those organisms or lineages with unclear taxonomical position. Although there may not be bad choices when selecting organisms for genome sequencing, there are certainly better choices if we aim to understand eukaryotic diversity. We argue that at least some of the effort should be specifically directed towards filling the gaps in the eukaryotic tree of life, focusing on those lineages that occupy key phylogenetic positions. How can that be done? One option is to sequence more cultured organisms. In fact, 95% of protist species in culture are not yet targeted for a genome project (Figure S1 in the supplementary data online). Thus, by obtaining the genome of some available cultured lineages that have not yet been sequenced, we could easily fill some of the important gaps of the tree, including some heterotrophic Stramenopila, Amoebozoa, and Rhizaria. However, selecting species that are available in culture is itself strongly biasing, and most lineages remain without any cultured representative [16del Campo J. et al.Culturing bias in marine heterotrophic flagellates analyzed through seawater enrichment incubations.Microb. Ecol. 2013; 66: 489-499Crossref PubMed Scopus (19) Google Scholar]. Publicly accessible protist collections [such as the American Type Culture Collection (ATCC) and the Culture Collection of Algae and Protozoa (CCAP); summarized in Box 2] are considerably smaller than their bacterial or fungal counterparts. Among the reasons is the lack of a required, systematic deposit of newly described taxa, in contrast to the situation for bacteria [17Lapage S.P. et al.International Code of Nomenclature of Bacteria. ASM Press, 1992http://www.ncbi.nlm.nih.gov/books/NBK8817/Google Scholar]. Notably, and unfortunately, half of the species with genome projects completed or in progress are not deposited in any of the five analyzed publicly accessible culture collections. To avoid more 'lost cultures' in the future the community should establish and adopt standard procedures similar to those used in bacteriology to release cultures to protist collections. The whole community will benefit from this in the short and long term. In addition, there is an inherent technical bias in culturing, as well as a bias in culturing efforts. For example, phototrophic representatives of Stramenopila and Alveolata tend to have more cultures available than their heterotrophic counterparts (Figure 4). Indeed, 70.6% of the most common protist strains present in culture collections are phototrophic organisms (Figure 3). Therefore there is a need both to increase the culturing effort for a wider variety of environments and to develop novel and alternative culture techniques to retrieve refractory organisms [18del Campo J. et al.Taming the smallest predators of the oceans.ISME J. 2013; 7: 351-358Crossref PubMed Scopus (33) Google Scholar], both of which take time, energy, and funding. Importantly, culture collections will need to be supported so that they can take on the challenge of maintaining more cultures and open their scope to include more difficult organisms that tend to be excluded from existing collections, in particular heterotrophs.Box 2Protist culture collectionsCulture collections are cornerstones for the development of all microbiological disciplines. Cultures are key to the establishment of model organisms and, therefore, to a better understanding of their biology. Below we describe some of the major protistan collections.ATCC (American Type Culture Collection; Manassas, Virginia, USA): a private, non-profit biological resource center established in 1925 with the aim of creating a central collection to supply microorganisms to scientists all over the world (http://www.atcc.org). ATCC collections include a great variety of biological materials such as cell lines, molecular genomics tools, microorganisms, and bioproducts. The microorganism collection includes more than 18 000 strains of bacteria, 3000 different types of viruses, over 49 000 yeast and fungal strains, and 2000 strains of protists.CCAP (Culture Collection of Algae and Protozoa; Oban, Scotland, UK): a culture collection funded by the UK Natural Environmental Research Centre (NERC) that contains algae and protozoa from both freshwater and marine environments. The foundations of CCAP (http://www.ccap.ac.uk) were laid by Prof. Ernst Georg Pringsheim and his collaborators and the cultures they established at the Botanical Institute of the German University of Prague in the 1920s. Pringsheim moved to England where the collection was expanded and taken over by Cambridge University in 1947. In 1970 these cultures formed the basis of the Culture Centre of Algae and Protozoa that later became the modern CCAP.NCMA (Provasoli-Guillard National Center for Marine Algae and Microbiota, East Boothbay, Maine, USA): this integrated collection of marine algae, protozoa, bacteria, archaea, and viruses was named a National Center and Facility by the US Congress in 1992. The NCMA (http://ncma.bigelow.org) originated from private culture collections established by Dr Luigi Provasoli at Yale University and Dr Robert R.L. Guillard at Woods Hole Oceanographic Institution. When it was born in the 1980s it was known as the Culture Collection of Marine Phytoplankton (CCMP) and provided to the community algal cultures of scientific interest or for aquaculture.RCC (Roscoff Culture Collection; Roscoff, France): this collection (http://www.roscoff-culture-collection.org) is located at the Station Biologique de Roscoff and is closely linked to the Oceanic Plankton group of this institution. They maintain more than 3000 strains of marine phytoplankton, especially picoplankton and picoeukaryotes from various oceanic regions. Most of the strains are available for distribution whereas others are in the process of being described.SAG (Sammlung von Algenkulturen: Culture Collection of Algae at Göttingen University, Göttingen, Germany): the SAG is a non-profit organization maintained by the University of Göttingen (http://www.epsag.uni-goettingen.de). The collection primarily contains microscopic algae and cyanobacteria from freshwater or terrestrial habitats, but there are also some marine algae. With more than 2400 strains, the SAG is among the three largest culture collections of algae in the world. Prof. Pringsheim is also the founder of the SAG: it was initiated in 1953 when he returned to Göttingen after his time as a refugee scientist in England. From then on the Pringsheim algal collection has been growing and evolving into the service collection we know nowadays. Culture collections are cornerstones for the development of all microbiological disciplines. Cultures are key to the establishment of model organisms and, therefore, to a better understanding of their biology. Below we describe some of the major protistan collections. ATCC (American Type Culture Collection; Manassas, Virginia, USA): a private, non-profit biological resource center established in 1925 with the aim of creating a central collection to supply microorganisms to scientists all over the world (http://www.atcc.org). ATCC collections include a great variety of biological materials such as cell li
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