Michael W. Gray

The Endosymbiont Hypothesis Revisited

Publisher Summary This chapter highlights endosymbiont hypothesis. All contemporary genomes (including those of plastids and mitochondria) ultimately derive from a single genome—the genome of a single, presumably cellular, entity which was the ancestor of all surviving forms of live. The construction and interpretation of phylogenetic trees based on small subunit (SSU, or 16S-like) and large subunit (LSU, or 23S-like) rRNA sequences have proven especially informative in instances where morphological diversity tends to confound traditional methods of phylogenetic analysis. In addition to ribosomal RNA (rRNA) sequence, there are a number of traits that characterize the archaebacteria as a distinct group of organisms, separate from all other prokaryotes. These include (1) cell walls that, when present, lack peptidoglycan and muramic acid; (2) the presence of lipids containing phytanyl side groups in ether linkage; and (3) the presence of RNA polymerases that are distinct from those of eubacteria in subunit composition, response to RNA synthesis inhibitors or stimulators, immunological reactivity, and gene sequence. Two major divisions of archaebacteria include (1) sulfur-dependent, extreme thermophiles; and (2) methane-producers (methanogens) and their relatives, including the extreme halophiles.

The origin and early evolution of mitochondria

Complete sequences of numerous mitochondrial, many prokaryotic, and several nuclear genomes are now available. These data confirm that the mitochondrial genome originated from a eubacterial (specifically α-proteobacterial) ancestor but raise questions about the evolutionary antecedents of the mitochondrial proteome.

The Closest Unicellular Relatives of Animals

Molecular phylogenies support a common ancestry between animals (Metazoa) and Fungi, but the evolutionary descent of the Metazoa from single-celled eukaryotes (protists) and the nature and taxonomic affiliation of these ancestral protists remain elusive. We addressed this question by sequencing complete mitochondrial genomes from taxonomically diverse protists to generate a large body of molecular data for phylogenetic analyses. Trees inferred from multiple concatenated mitochondrial protein sequences demonstrate that animals are specifically affiliated with two morphologically dissimilar unicellular protist taxa: Monosiga brevicollis (Choanoflagellata), a flagellate, and Amoebidium parasiticum (Ichthyosporea), a fungus-like organism. Statistical evaluation of competing evolutionary hypotheses confirms beyond a doubt that Choanoflagellata and multicellular animals share a close sister group relationship, originally proposed more than a century ago on morphological grounds. For the first time, our trees convincingly resolve the currently controversial phylogenetic position of the Ichthyosporea, which the trees place basal to Choanoflagellata and Metazoa but after the divergence of Fungi. Considering these results, we propose the new taxonomic group Holozoa, comprising Ichthyosporea, Choanoflagellata, and Metazoa. Our findings provide insight into the nature of the animal ancestor and have broad implications for our understanding of the evolutionary transition from unicellular protists to multicellular animals.

The evolutionary origins of organelles

Analysis of organellar genomes strongly supports the idea that chloroplasts and mitochondria originated in evolution as eubacteria-like endosymbionts, whose closest contemporaries are cyanobacteria and purple photosynthetic bacteria, respectively. However, there is still much debate about whether a single endosymbiotic event or multiple ones gave rise to each organelle in different eukaryotes, and considerable uncertainty about what has happened to the genomes of chloroplasts and mitochondria since their appearance in the eukaryotic cell.

Origin and ,evolution of organelle genomes

Molecular data (particularly sequence analyses) have established that two eukaryotic organelles, the mitochondrion and the plastid, are the descendants of endosymbiotic (eu)bacteria whose closest living relatives are the alpha-Proteobacteria (mitochondrion) and Cyanobacteria (plastid). This review describes recent data that favor the view that each organelle arose via this primary endosymbiotic pathway only once (monophyletic origin), such as the discovery of group I introns that appear to be structurally homologous and have identical insertion sites in metaphyte, chlorophyte and fungal mitochondrial genomes. However, it is also evident that the plastids in certain algal groups were acquired secondarily through a eukaryotic rather than a prokaryotic endosymbiont.

AutoFACT: An Automatic Functional Annotation and Classification Tool

BackgroundAssignment of function to new molecular sequence data is an essential step in genomics projects. The usual process involves similarity searches of a given sequence against one or more databases, an arduous process for large datasets.ResultsWe present AutoFACT, a fully automated and customizable annotation tool that assigns biologically informative functions to a sequence. Key features of this tool are that it (1) analyzes nucleotide and protein sequence data; (2) determines the most informative functional description by combining multiple BLAST reports from several user-selected databases; (3) assigns putative metabolic pathways, functional classes, enzyme classes, GeneOntology terms and locus names; and (4) generates output in HTML, text and GFF formats for the users convenience. We have compared AutoFACT to four well-established annotation pipelines. The error rate of functional annotation is estimated to be only between 1–2%. Comparison of AutoFACT to the traditional top-BLAST-hit annotation method shows that our procedure increases the number of functionally informative annotations by approximately 50%.ConclusionAutoFACT will serve as a useful annotation tool for smaller sequencing groups lacking dedicated bioinformatics staff. It is implemented in PERL and runs on LINUX/UNIX platforms. AutoFACT is available at http://megasun.bch.umontreal.ca/Software/AutoFACT.htm.

COMPLETE SEQUENCE OF THE MITOCHONDRIAL DNA OF THE RED ALGA PORPHYRA PURPUREA : CYANOBACTERIAL INTRONS AND SHARED ANCESTRY OF RED AND GREEN ALGAE

The mitochondrial DNA (mtDNA) of Porphyra purpurea, a circular-mapping genome of 36,753 bp, has been completely sequenced. A total of 57 densely packed genes has been identified, including the basic set typically found in animals and fungi, as well as seven genes characteristic of protist and plant mtDNAs and specifying ribosomal proteins and subunits of succinate:ubiquinone oxido-reductase. The mitochondrial large subunit rRNA gene contains two group II introns that are extraordinarily similar to those found in the cyanobacterium Calothrix sp, suggesting a recent lateral intron transfer between a bacterial and a mitochondrial genome. Notable features of P. purpurea mtDNA include the presence of two 291-bp inverted repeats that likely mediate homologous recombination, resulting in genome rearrangement, and of numerous sequence polymorphisms in the coding and intergenic regions. Comparative analysis of red algal mitochondrial genomes from five different, evolutionarily distant orders reveals that rhodophyte mtDNAs are unusually uniform in size and gene order. Finally, phylogenetic analyses provide strong evidence that red algae share a common ancestry with green algae and plants.

The Complete Mitochondrial DNA Sequences of Nephroselmis olivacea and Pedinomonas minor : Two Radically Different Evolutionary Patterns within Green Algae

Green plants appear to comprise two sister lineages, Chlorophyta (classes Chlorophyceae, Ulvophyceae, Trebouxiophyceae, and Prasinophyceae) and Streptophyta (Charophyceae and Embryophyta, or land plants). To gain insight into the nature of the ancestral green plant mitochondrial genome, we have sequenced the mitochondrial DNAs (mtDNAs) of Nephroselmis olivacea and Pedinomonas minor. These two green algae are presumptive members of the Prasinophyceae. This class is thought to include descendants of the earliest diverging green algae. We find that Nephroselmis and Pedinomonas mtDNAs differ markedly in size, gene content, and gene organization. Of the green algal mtDNAs sequenced so far, that of Nephroselmis (45,223 bp) is the most ancestral (minimally diverged) and occupies the phylogenetically most basal position within the Chlorophyta. Its repertoire of 69 genes closely resembles that in the mtDNA of Prototheca wickerhamii, a later diverging trebouxiophycean green alga. Three of the Nephroselmis genes (nad10, rpl14, and rnpB) have not been identified in previously sequenced mtDNAs of green algae and land plants. In contrast, the 25,137-bp Pedinomonas mtDNA contains only 22 genes and retains few recognizably ancestral features. In several respects, including gene content and rate of sequence divergence, Pedinomonas mtDNA resembles the reduced mtDNAs of chlamydomonad algae, with which it is robustly affiliated in phylogenetic analyses. Our results confirm the existence of two radically different patterns of mitochondrial genome evolution within the green algae.

The Evolutionary Relationships among Known Life Forms

SummarySequences of small subunit (SSU) and large subunit (LSU) ribosomal RNA genes from archaebacteria, eubacteria, and the nucleus, chloroplasts, and mitochondria of eukaryotes have been compared in order to identify the most conservative positions. Aligned sets of these positions for both SSU and LSU rRNA have been used to generate tree diagrams relating the source organisms/organelles. Branching patterns were evaluated using the statistical bootstrapping technique. The resulting SSU and LSU trees are remarkably congruent and show a high degree of similarity with those based on alternative data sets and/or generated by different techniques. In addition to providing insights into the evolution of prokaryotic and eukaryotic (nuclear) lineages, the analysis reported here provides, for the first time, an extensive phylogeny of the mitochondrial lineage.

Evolutionary biology: Mitochondrial genes on the move

In flowering plants, genes have frequently been transferred from mitochondria to the cell nucleus by way of a remarkable evolutionary rapid-transit system.