Chapter Five - The Ectocarpus Genome and Brown Algal Genomics: The Ectocarpus Genome Consortium
Introduction
Brown algae (or Phaeophyceae) are a group of multicellular algae that belong to the stramenopile lineage (also known as heterokonts). They occur almost exclusively in marine environments, particularly rocky coastlines in temperate regions of the globe. Brown algae are often the main primary producers of such ecosystems and therefore play an important ecological role, creating habitats for a broad range of other marine organisms. As a consequence, there has been considerable interest in understanding the biology and ecology of the brown algae. These organisms have also attracted interest for a number of other reasons. The stramenopiles are very distantly related to well-studied groups such as the opisthokonts (animals and fungi) and the green lineage (which includes land plants); the common ancestor of these major lineages dating back to the crown radiation of the eukaryotes more than a billion years ago (Yoon, Hackett, Ciniglia, Pinto & Bhattacharya, 2004). During this long period of evolutionary time, the brown algae have evolved many unusual characteristics that are not found in the other groups, including a number of features that have exquisitely adapted these organisms for the harsh environment of the intertidal and subtidal zones. Brown algae exhibit novel features even at the basic level of their cell biology. For example, they acquired their plastid via a process of secondary endosymbiosis involving the capture of a red alga (Archibald, 2012, in this volume; Keeling, 2004), an event that had a major consequence both on the ultrastructure of the cell and on the composition of the nuclear genome (as a result of gene transfers from the endosymbiont). Brown algae are also remarkable in that they are one of only a small number of eukaryotic groups to have evolved complex multicellularity (Cock et al., 2010).
Over the past two decades, the adoption of genomic approaches such as genome sequencing and efficient methods to analyse gene function has allowed remarkable progress in our understanding of the biology of selected model organisms in the animal, plant and fungal lineages. During this time, it became clear that it would be necessary to select an analogous model organism for the brown algae if similar approaches were to be applied to this group. In 2004, several potential brown algal model species were compared, leading to a proposition to develop genomic and genetic tools and techniques for the filamentous brown alga Ectocarpus (Fig. 5.1; Peters, Marie, Scornet, Kloareg & Cock, 2004). Ectocarpus was selected because mature thalli are small, highly fertile and progress rapidly through the life cycle (Müller, Kapp & Knippers, 1998), characteristics that are essential for the application of genetic approaches. It had also been shown that basic genetic methods such as crosses and segregation analysis could be used with this organism (Bräutigam, Klein, Knippers & Müller, 1995) and axenic cultures can be established (Müller, Gachon & Küpper, 2008). In addition, several aspects of the biology of Ectocarpus had been studied, including taxonomy, life cycle, different aspects of cell biology and metabolism and responses to biotic and abiotic stresses (Charrier et al., 2008).
One of the key steps towards the emergence of Ectocarpus as a model organism was the development of a complete genome sequencing project for this organism. This project, which involved more than 30 laboratories, was initiated in 2006 and was completed with the publication of the genome sequence in 2010 (Cock et al., 2010). The following sections describe the many interesting features of this genome and the insights into brown algal biology that analysis of the genome has afforded.
The Ectocarpus genome sequence was obtained using strain Ec32, which is a male meiotic offspring of a field sporophyte collected in 1988 in San Juan de Marcona, Peru (Peters et al., 2008). Initially considered to belong to the species E. siliculosus, more recent phylogenetic analyses suggest that strain Ec32 belongs to a so far unnamed species of the same genus (Peters et al., 2010a). The size of the genome in this strain had been estimated at 214 Mbp using flow cytometry (Peters et al., 2004) and the length of the assembled genome sequence, which comprised 1561 supercontigs of greater than 2 kbp, was consistent with this estimation (Cock et al., 2010). A sequence-anchored genetic map was used to assign 325 of the longest supercontigs (137 Mbp or 70% of the genome) to linkage groups and thereby produce a large-scale assembly of the genome sequence by concatenating supercontigs to produce pseudochromosomes (Heesch et al., 2010). The number of linkage groups (26 major and 8 minor linkage groups) is consistent with previous estimates of chromosome number based on cytogenetic studies (Müller, 1966, Müller, 1967) if we assume that the eight minor linkage groups represent fragments that should be associated with the larger groups.
Section snippets
Large-scale Structure
Analysis of gene and transposon density along the Ectocarpus pseudochromosome sequences did not reveal any obvious large-scale structures that could have represented centromeres or heterochromatic knobs, although it is possible that such regions were lost during the assembly stage if they are very rich in repeated sequences. Linkage group 30 was particularly rich in transposons and poor in genes compared to the other major linkage groups. No evidence was found for large-scale duplication events
Evolution of Genome Gene Content
Several approaches have been used to compare the inventory of proteins encoded by the Ectocarpus genome (the proteome) with those of other organisms in an effort to understand the evolutionary history of the genome (Cock et al., 2010). These have included comparisons with complete proteomes from other stramenopiles, blast comparisons with the National Center for Biotechnology Information database and a reconstruction of gene family loss and gain during evolution using Dollo logic (Cock et al.,
Photosynthesis and Photosynthetic Pigments
The Ectocarpus light reaction and electron transport system gene complements are very similar to those of green plants, except for the lack of plastocyanin, which is usually replaced by cytochrome c6 in chromist algae. More chlorophyll-binding protein (CBP) genes were found in the Ectocarpus genome than in any green plant genome studied to date (Dittami, Michel, Collen, Boyen & Tonon, 2010), suggesting that Ectocarpus employs a complex repertoire of CBP genes in order to cope with the
Receptors, Ion Channels and Signal Transduction Pathways
The Ectocarpus genome provided evidence for several types of sensor molecule, including molecules located both on the cell membrane and within the cytoplasm (Cock et al., 2010). These included molecules that have been found in other stramenopiles, such as G-protein-coupled receptors and their associated heterotrimeric G-proteins, and molecules that have so-far appeared to be absent from chromalveolates, such as membrane-located histidine kinases. The Ectocarpus genome encodes three
Future Directions
Analysis of the Ectocarpus genome sequence has provided a large amount of information about the probable molecular systems that underlie a broad range of processes in brown algae. However, this information is based principally on parallels with other organisms (sequence homology) and an important challenge for the future will be to develop methods of directly investigating gene function in Ectocarpus. These methods need to include not only ways of disrupting gene function but also tools to
Acknowledgements
Work on Ectocarpus has been supported by the Centre National de la Recherche Scientifique, the University Pierre and Marie Curie, the Inter-University Network for Fundamental Research (P6/25, BioMaGNet), the Europole Mer, the European Union Infrastructures program (project Assemble), the Interreg program France (Channel)-England (project Marinexus), the Agence Nationale de la Recherche (project Bi-cycle) and Natural Environment Research Council (United Kingdom) grants NE/F012705/1 and
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