The GC-rich mitochondrial and plastid genomes of the green alga Coccomyxa give insight into the evolution of organelle DNA nucleotide landscape.
ABSTRACT: Most of the available mitochondrial and plastid genome sequences are biased towards adenine and thymine (AT) over guanine and cytosine (GC). Examples of GC-rich organelle DNAs are limited to a small but eclectic list of species, including certain green algae. Here, to gain insight in the evolution of organelle nucleotide landscape, we present the GC-rich mitochondrial and plastid DNAs from the trebouxiophyte green alga Coccomyxa sp. C-169. We compare these sequences with other GC-rich organelle DNAs and argue that the forces biasing them towards G and C are nonadaptive and linked to the metabolic and/or life history features of this species. The Coccomyxa organelle genomes are also used for phylogenetic analyses, which highlight the complexities in trying to resolve the interrelationships among the core chlorophyte green algae, but ultimately favour a sister relationship between the Ulvophyceae and Chlorophyceae, with the Trebouxiophyceae branching at the base of the chlorophyte crown.
Project description:The mitochondrial genomes of chlamydomonadalean green algae are renowned for their highly reduced and conserved gene repertoires, which are almost fixed at 12 genes across the entire lineage. The sizes of these genomes, however, are much more variable, with some species having small, compact mitochondrial DNAs (mtDNAs) and others having expanded ones. Earlier work demonstrated that the halophilic genus Dunaliella contains extremely inflated organelle genomes, but to date the mtDNA of only one isolate has been explored. Here, by surveying mtDNA architecture across the Chlamydomonadales, we show that various Dunaliella species have undergone massive levels of mitochondrial genomic expansion, harboring the most inflated, intron-dense mtDNAs available from chlorophyte green algae. The same also appears to be true for their plastid genomes, which are potentially among the largest of all plastid-containing eukaryotes. Genetic divergence data are used to investigate the underlying causes of such extreme organelle genomic architectures, and ultimately reveal order-of-magnitude differences in mitochondrial versus plastid mutation rates within Dunaliella.
Project description:We report the complete organelle genome sequences of Trebouxiophyceae sp. strain MX-AZ01, an acidophilic green microalga isolated from a geothermal field in Mexico. This eukaryote has the remarkable ability to thrive in a particular shallow lake with emerging hot springs at the bottom, extremely low pH, and toxic heavy metal concentrations. Trebouxiophyceae sp. MX-AZ01 represents one of few described photosynthetic eukaryotes living in such a hostile environment. The organelle genomes of Trebouxiophyceae sp. MX-AZ01 are remarkable. The plastid genome sequence currently presents the highest G+C content for a trebouxiophyte. The mitochondrial genome sequence is the largest reported to date for the Trebouxiophyceae class of green algae. The analysis of the genome sequences presented here provides insight into the evolution of organelle genomes of trebouxiophytes and green algae.
Project description:In this data article, information is provided on sequences of KT-HAK-KUP transporters from green algae and basal land plants. A data set is offered containing sequences corresponding to the chlorophyte algae Chlamydomonas eustigma, Gonium pectorale and Coccomyxa subellipsoidea, the charophyte algae Coleochaete orbicularis and Klebsormidium flaccidum, the bryophyte Sphagnum fallax, the marchantophyte Marchantia polymorpha and the gymnosperm Pinus taeda, which have been not formerly analyzed. In addition, an analysis of similarity scores among representatives of the clusters recognized in photosynthetic green organisms (namely, chlorophyte algae, charophyte algae, basal embryophytes and higher embryophytes) is performed as well as an analysis of membrane topology for them.
Project description:Volvocalean green algae have among the most diverse mitochondrial and plastid DNAs (mtDNAs and ptDNAs) from the eukaryotic domain. However, nearly all of the organelle genome data from this group are restricted to unicellular species, like Chlamydomonas reinhardtii, and presently only one multicellular species, the ?4,000-celled Volvox carteri, has had its organelle DNAs sequenced. The V. carteri organelle genomes are repeat rich, and the ptDNA is the largest plastome ever sequenced. Here, we present the complete mtDNA and ptDNA of the colonial volvocalean Gonium pectorale, which is comprised of ?16 cells and occupies a phylogenetic position closer to that of V. carteri than C. reinhardtii within the volvocine line. The mtDNA and ptDNA of G. pectorale are circular-mapping AT-rich molecules with respective lengths and coding densities of 16 and 222.6 kilobases and 73 and 44%. They share some features with the organelle DNAs of V. carteri, including palindromic repeats within the plastid compartment, but show more similarities with those of C. reinhardtii, such as a compact mtDNA architecture and relatively low organelle DNA intron contents. Overall, the G. pectorale organelle genomes raise several interesting questions about the origin of linear mitochondrial chromosomes within the Volvocales and the relationship between multicellularity and organelle genome expansion.
Project description: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 ( approximately 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.
Project description:BACKGROUND:Dunaliella salina Teodoresco, a unicellular, halophilic green alga belonging to the Chlorophyceae, is among the most industrially important microalgae. This is because D. salina can produce massive amounts of beta-carotene, which can be collected for commercial purposes, and because of its potential as a feedstock for biofuels production. Although the biochemistry and physiology of D. salina have been studied in great detail, virtually nothing is known about the genomes it carries, especially those within its mitochondrion and plastid. This study presents the complete mitochondrial and plastid genome sequences of D. salina and compares them with those of the model green algae Chlamydomonas reinhardtii and Volvox carteri. RESULTS:The D. salina organelle genomes are large, circular-mapping molecules with approximately 60% noncoding DNA, placing them among the most inflated organelle DNAs sampled from the Chlorophyta. In fact, the D. salina plastid genome, at 269 kb, is the largest complete plastid DNA (ptDNA) sequence currently deposited in GenBank, and both the mitochondrial and plastid genomes have unprecedentedly high intron densities for organelle DNA: approximately 1.5 and approximately 0.4 introns per gene, respectively. Moreover, what appear to be the relics of genes, introns, and intronic open reading frames are found scattered throughout the intergenic ptDNA regions -- a trait without parallel in other characterized organelle genomes and one that gives insight into the mechanisms and modes of expansion of the D. salina ptDNA. CONCLUSIONS:These findings confirm the notion that chlamydomonadalean algae have some of the most extreme organelle genomes of all eukaryotes. They also suggest that the events giving rise to the expanded ptDNA architecture of D. salina and other Chlamydomonadales may have occurred early in the evolution of this lineage. Although interesting from a genome evolution standpoint, the D. salina organelle DNA sequences will aid in the development of a viable plastid transformation system for this model alga, and they will complement the forthcoming D. salina nuclear genome sequence, placing D. salina in a group of a select few photosynthetic eukaryotes for which complete genome sequences from all three genetic compartments are available.
Project description:The tiny green algae belonging to the Chloropicophyceae play a key role in marine phytoplankton communities; this newly erected class of prasinophytes comprises two genera (Chloropicon and Chloroparvula) containing each several species. We sequenced the plastomes and mitogenomes of eight Chloropicon and five Chloroparvula species to better delineate the phylogenetic affinities of these taxa and to infer the suite of changes that their organelle genomes sustained during evolution. The relationships resolved in organelle-based phylogenomic trees were essentially congruent with previously reported rRNA trees, and similar evolutionary trends but distinct dynamics were identified for the plastome and mitogenome. Although the plastome sustained considerable changes in gene content and order at the time the two genera split, subsequently it remained stable and maintained a very small size. The mitogenome, however, was remodeled more gradually and showed more fluctuation in size, mainly as a result of expansions/contractions of intergenic regions. Remarkably, the plastome and mitogenome lost a common set of three tRNA genes, with the trnI(cau) and trnL(uaa) losses being accompanied with important variations in codon usage. Unexpectedly, despite the disappearance of trnI(cau) from the plastome in the Chloroparvula lineage, AUA codons (the codons recognized by this gene product) were detected in certain plastid genes. By comparing the sequences of plastid protein-coding genes from chloropicophycean and phylogenetically diverse chlorophyte algae with those of the corresponding predicted proteins, we discovered that the AUA codon was reassigned from isoleucine to methionine in Chloroparvula. This noncanonical genetic code has not previously been uncovered in plastids.
Project description:Plastid genomes are not normally celebrated for being large. But researchers are steadily uncovering algal lineages with big and, in rare cases, enormous plastid DNAs (ptDNAs), such as volvocine green algae. Plastome sequencing of five different volvocine species has revealed some of the largest, most repeat-dense plastomes on record, including that of Volvox carteri (?525?kb). Volvocine algae have also been used as models for testing leading hypotheses on organelle genome evolution (e.g., the mutational hazard hypothesis), and it has been suggested that ptDNA inflation within this group might be a consequence of low mutation rates and/or the transition from a unicellular to multicellular existence. Here, we further our understanding of plastome size variation in the volvocine line by examining the ptDNA sequences of the colonial species Yamagishiella unicocca and Eudorina sp. NIES-3984 and the multicellular Volvox africanus, which are phylogenetically situated between species with known ptDNA sizes. Although V. africanus is closely related and similar in multicellular organization to V. carteri, its ptDNA was much less inflated than that of V. carteri. Synonymous- and noncoding-site nucleotide substitution rate analyses of these two Volvox ptDNAs suggest that there are drastically different plastid mutation rates operating in the coding versus intergenic regions, supporting the idea that error-prone DNA repair in repeat-rich intergenic spacers is contributing to genome expansion. Our results reinforce the idea that the volvocine line harbors extremes in plastome size but ultimately shed doubt on some of the previously proposed hypotheses for ptDNA inflation within the lineage.
Project description:Protein-coding genes in organellar genomes have been widely used to resolve relationships of chlorophyte algae. The mode of evolution of these protein-coding genes affects relationship estimations, yet selection effects on genes commonly used as markers in phylogenetic analyses are insufficiently well understood. To gain more understanding about the effects of green algal organelle protein-coding genes on phylogenies, more information is needed about the mode of gene evolution. We used phylogenetic frameworks to examine evolutionary relationships of 58 protein-coding genes present in the organellar genomes of chlorophyte and streptophyte algae at multiple levels: organelle, biological function, and individual gene, and calculated pairwise dN/dS ratios of algal organellar protein-coding genes to investigate mode of evolution. Results indicate that mitochondrial genes have evolved at a higher rate than have chloroplast genes. Low dN/dS ratios indicating relatively high level of conservation indicate that nad2, nad5, atpA, atpE, psbC, and psbD might be particularly good candidates for use as markers in chlorophyte phylogenies. Chlorophycean atp6, nad2, atpF, clpP, rps2, rps3, rps4, and rps7 protein-coding sequences exhibited selective mutations, suggesting that changes in proteins encoded by these genes might have increased fitness in Chlorophyceae.
Project description:Algae are the oldest taxa on Earth, with an evolutionary relationship that spans prokaryotes (Cyanobacteria) and eukaryotes. A long evolutionary history has led to high algal diversity. Their organelle DNAs are characterized by uniparental inheritance and a compact genome structure compared with nuclear genomes; thus, they are efficient molecular tools for the analysis of gene structure, genome structure, organelle function and evolution. However, an integrated organelle genome database for algae, which could enable users to both examine and use relevant data, has not previously been developed. Therefore, to provide an organelle genome platform for algae, we have developed a user-friendly database named Organelle Genome Database for Algae (OGDA, http://ogda.ytu.edu.cn/). OGDA contains organelle genome data either retrieved from several public databases or sequenced in our laboratory (Laboratory of Genetics and Breeding of Marine Organism [MOGBL]), which are continuously updated. The first release of OGDA contains 1055 plastid genomes and 755 mitochondrial genomes. Additionally, a variety of applications have been integrated into this platform to analyze the structural characteristics, collinearity and phylogeny of organellar genomes for algae. This database represents a useful tool for users, enabling the rapid retrieval and analysis of information related to organellar genomes for biological discovery.