John M. Archibald

The Puzzle of Plastid Evolution

A comprehensive understanding of the origin and spread of plastids remains an important yet elusive goal in the field of eukaryotic evolution. Combined with the discovery of new photosynthetic and non-photosynthetic protist lineages, the results of recent taxonomically broad phylogenomic studies suggest that a re-shuffling of higher-level eukaryote systematics is in order. Consequently, new models of plastid evolution involving ancient secondary and tertiary endosymbioses are needed to explain the full spectrum of photosynthetic eukaryotes.

The Marine Microbial Eukaryote Transcriptome Sequencing Project (MMETSP): Illuminating the Functional Diversity of Eukaryotic Life in the Oceans through Transcriptome Sequencing.

Current sampling of genomic sequence data from eukaryotes is relatively poor, biased, and inadequate to address important questions about their biology, evolution, and ecology; this Community Page describes a resource of 700 transcriptomes from marine microbial eukaryotes to help understand their role in the worlds oceans.

Lateral gene transfer and the evolution of plastid-targeted proteins in the secondary plastid-containing alga Bigelowiella natans

Chlorarachniophytes are amoeboflagellate algae that acquired photosynthesis secondarily by engulfing a green alga and retaining its plastid (chloroplast). An important consequence of secondary endosymbiosis in chlorarachniophytes is that most of the nuclear genes encoding plastid-targeted proteins have moved from the nucleus of the endosymbiont to the host nucleus. We have sequenced and analyzed 83 cDNAs encoding 78 plastid-targeted proteins from the model chlorarachniophyte Bigelowiella natans (formerly Chlorarachnion sp. CCMP621). Phylogenies inferred from the majority of these genes are consistent with a chlorophyte green algal origin. However, a significant number of genes (≈21%) show signs of having been acquired by lateral gene transfer from numerous other sources: streptophyte algae, red algae (or algae with red algal endosymbionts), as well as bacteria. The chlorarachniophyte plastid proteome may therefore be regarded as a mosaic derived from various organisms in addition to the ancestral chlorophyte plastid. In contrast, the homologous genes from the chlorophyte Chlamydomonas reinhardtii do not show any indications of lateral gene transfer. This difference is likely a reflection of the mixotrophic nature of Bigelowiella (i.e., it is photosynthetic and phagotrophic), whereas Chlamydomonas is strictly autotrophic. These results underscore the importance of lateral gene transfer in contributing foreign proteins to eukaryotic cells and their organelles, and also suggest that its impact can vary from lineage to lineage.

Recycled plastids: a ‘green movement’ in eukaryotic evolution

Secondary endosymbiosis is the process that drives the spread of plastids (chloroplasts) from one eukaryote to another. The number of times that this has occurred and the kinds of cells involved are now becoming clear. Reconstructions of plastid history using molecular data suggest that secondary endosymbiosis is very rare and that perhaps as few as three endosymbioses have resulted in a large proportion of algal diversity. The significance of these events extends beyond photosynthesis, however, because non-photosynthetic organisms such as ciliates appear to have evolved from photosynthetic ancestors and could still harbor plastid-derived genes or relict plastids.

Diversity, Nomenclature, and Taxonomy of Protists

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MKKS/BBS6, a divergent chaperonin-like protein linked to the obesity disorder Bardet-Biedl syndrome, is a novel centrosomal component required for cytokinesis

Chaperonins are multisubunit, cylinder-shaped molecular chaperones involved in folding newly synthesized polypeptides. Here we show that MKKS/BBS6, one of several proteins associated with Bardet-Biedl syndrome (BBS), is a Group II chaperonin-like protein that has evolved recently in animals from a subunit of the eukaryotic chaperonin CCT/TRiC, and diverged rapidly to acquire distinct functions. Unlike other chaperonins, cytosolic BBS6 does not oligomerize, and the majority of BBS6 resides within the pericentriolar material (PCM), a proteinaceous tube surrounding centrioles. During interphase, BBS6 is confined to the lateral surfaces of the PCM but during mitosis it relocalizes throughout the PCM and is found at the intercellular bridge. Its predicted substrate-binding apical domain is sufficient for centrosomal association, and several patient-derived mutations in this domain cause mislocalization of BBS6. Consistent with an important centrosomal function, silencing of the BBS6 transcript by RNA interference in different cell types leads to multinucleate and multicentrosomal cells with cytokinesis defects. The restricted tissue distribution of BBS6 further suggests that it may play important roles in ciliated epithelial tissues, which is consistent with the probable functions of BBS proteins in basal bodies (modified centrioles) and cilia. Our findings provide the first insight into the nature and cellular function of BBS6, and shed light on the potential causes of several ailments, including obesity, retinal degeneration, kidney dysfunction and congenital heart disease.

Large-Scale Phylogenomic Analyses Reveal That Two Enigmatic Protist Lineages, Telonemia and Centroheliozoa, Are Related to Photosynthetic Chromalveolates

Understanding the early evolution and diversification of eukaryotes relies on a fully resolved phylogenetic tree. In recent years, most eukaryotic diversity has been assigned to six putative supergroups, but the evolutionary origin of a few major “orphan” lineages remains elusive. Two ecologically important orphan groups are the heterotrophic Telonemia and Centroheliozoa. Telonemids have been proposed to be related to the photosynthetic cryptomonads or stramenopiles and centrohelids to haptophytes, but molecular phylogenies have failed to provide strong support for any phylogenetic hypothesis. Here, we investigate the origins of Telonema subtilis (a telonemid) and Raphidiophrys contractilis (a centrohelid) by large-scale 454 pyrosequencing of cDNA libraries and including new genomic data from two cryptomonads (Guillardia theta and Plagioselmis nannoplanctica) and a haptophyte (Imantonia rotunda). We demonstrate that 454 sequencing of cDNA libraries is a powerful and fast method of sampling a high proportion of protist genes, which can yield ample information for phylogenomic studies. Our phylogenetic analyses of 127 genes from 72 species indicate that telonemids and centrohelids are members of an emerging major group of eukaryotes also comprising cryptomonads and haptophytes. Furthermore, this group is possibly closely related to the SAR clade comprising stramenopiles (heterokonts), alveolates, and Rhizaria. Our results link two additional heterotrophic lineages to the predominantly photosynthetic chromalveolate supergroup, providing a new framework for interpreting the evolution of eukaryotic cell structures and the diversification of plastids.

Cell biology. Irremediable complexity

Complex cellular machines may have evolved through a ratchet-like process called constructive neutral evolution. Many of the cells macromolecular machines appear gratuitously complex, comprising more components than their basic functions seem to demand. How can we make sense of this complexity in the light of evolution? One possibility is a neutral ratchet-like process described more than a decade ago (1), subsequently called constructive neutral evolution (2). This model provides an explanatory counterpoint to the selectionist or adaptationist views that pervade molecular biology (3).

Nucleomorph genome of Hemiselmis andersenii reveals complete intron loss and compaction as a driver of protein structure and function

Nucleomorphs are the remnant nuclei of algal endosymbionts that took up residence inside a nonphotosynthetic eukaryotic host. The nucleomorphs of cryptophytes and chlorarachniophytes are derived from red and green algal endosymbionts, respectively, and represent a stunning example of convergent evolution: their genomes have independently been reduced and compacted to <1 megabase pairs (Mbp) in size (the smallest nuclear genomes known) and to a similar three-chromosome architecture. The molecular processes underlying genome reduction and compaction in eukaryotes are largely unknown, as is the impact of reduction/compaction on protein structure and function. Here, we present the complete 0.572-Mbp nucleomorph genome of the cryptophyte Hemiselmis andersenii and show that it is completely devoid of spliceosomal introns and genes for splicing RNAs—a case of complete intron loss in a nuclear genome. Comparison of H. andersenii proteins to those encoded in the slightly smaller (0.551-Mbp) nucleomorph genome of another cryptophyte, Guillardia theta, and to their homologs in the unicellular red alga Cyanidioschyzon merolae reveal that (i) cryptophyte nucleomorph genomes encode proteins that are significantly smaller than those in their free-living algal ancestors, and (ii) the smaller, more compact G. theta nucleomorph genome encodes significantly smaller proteins than that of H. andersenii. These results indicate that genome compaction can eliminate both coding and noncoding DNA and, consequently, drive the evolution of protein structure and function. Nucleomorph proteins have the potential to reveal the minimal functional units required for basic eukaryotic cellular processes.

Endosymbiosis and Eukaryotic Cell Evolution.

Understanding the evolution of eukaryotic cellular complexity is one of the grand challenges of modern biology. It has now been firmly established that mitochondria and plastids, the classical membrane-bound organelles of eukaryotic cells, evolved from bacteria by endosymbiosis. In the case of mitochondria, evidence points very clearly to an endosymbiont of α-proteobacterial ancestry. The precise nature of the host cell that partnered with this endosymbiont is, however, very much an open question. And while the host for the cyanobacterial progenitor of the plastid was undoubtedly a fully-fledged eukaryote, how - and how often - plastids moved from one eukaryote to another during algal diversification is vigorously debated. In this article I frame modern views on endosymbiotic theory in a historical context, highlighting the transformative role DNA sequencing played in solving early problems in eukaryotic cell evolution, and posing key unanswered questions emerging from the age of comparative genomics.