Multiple microalgal partners in symbiosis with the acantharian Acanthochiasma sp. (Radiolaria)

Acantharia (Radiolaria) are widespread and abundant heterotrophic marine protists, some of which can host endosymbiotic eukaryotic microalgae. Although this photosymbiotic association was first described at the end of the 19th century, the diversity of the symbiotic microalgae remains poorly characterized. Here, we examined the identity of the microalgae associated with the acantharian species Acanthochiasma sp. by sequencing partial 18S and internal transcribed spacer (ITS) ribosomal DNA genes from cultured symbionts and directly from isolated holobiont specimens. Single Acanthochiasma cells contained multiple symbiotic partners, including distantly related dinoflagellates (Heterocapsa sp., Pelagodinium sp., Azadinium sp. and Scrippsiella sp.) as well as a haptophyte (Chrysochromulina sp.). This original association of multiple symbiotic microalgae within a single host cell raises questions about the specificity and functioning of the relationship. These microalgae exhibit the common ecological feature of being abundant and widely distributed in coastal and oceanic waters, some occasionally forming extensive blooms. Some of the microalgal genera found in association with Acanthochiasma (i.e. Pelagodinium and Chrysochromulina) are known to occur in symbiosis with other heterotrophic protists such as Foraminifera and other Radiolaria, whereas Heterocapsa, Scrippsiella and Azadinium have never previously been reported to be involved in putative symbiotic relationships. The unusual association unveiled in this study contributes to our understanding of the ecological and evolutionary significance of photosymbiosis in Acantharia and also provides new insights into the nature of such partnerships in the planktonic realm.     

Cryptic Sex in Symbiodinium (Alveolata,Dinoflagellata) is Supported by an Inventory of Meiotic Genes

Symbiodinium encompasses a diverse clade of dinoflagellates that are ecologically important as symbionts of corals and other marine organisms. Despite decades of study, cytological evidence of sex (karyogamy and meiosis) has not been demonstrated in Symbiodinium, although molecular population genetic patterns support the occurrence of sexual recombination. Here, we provide additional support for sex in Symbiodinium by uncovering six meiosis‐specific and 25 meiosis‐related genes in three published genomes. Cryptic sex may be occurring in Symbiodinium's seldom‐seen free‐living state while being inactive in the symbiotic state.     

Differential stability of photosynthetic membranes and fatty acid composition at elevated temperature in Symbiodinium

Coral reefs are threatened by increasing surface seawater temperatures resulting from climate change. Reef-building corals symbiotic with dinoflagellates in the genus Symbiodinium experience dramatic reductions in algal densities when exposed to temperatures above the long-term local summer average, leading to a phenomenon called coral bleaching. Although the temperature-dependent loss in photosynthetic function of the algal symbionts has been widely recognized as one of the early events leading to coral bleaching, there is considerable debate regarding the actual damage site. We have tested the relative thermal stability and composition of membranes in Symbiodinium exposed to high temperature. Our results show that melting curves of photosynthetic membranes from different symbiotic dinoflagellates substantiate a species-specific sensitivity to high temperature, while variations in fatty acid composition under high temperature rather suggest a complex process in which various modifications in lipid composition may be involved. Our results do not support the role of unsaturation of fatty acids of the thylakoid membrane as being mechanistically involved in bleaching nor as being a dependable tool for the diagnosis of thermal susceptibility of symbiotic reef corals.     

Dot1-Dependent Histone H3K79 Methylation Promotes the Formation of Meiotic Double-Strand Breaks in the Absence of Histone H3K4 Methylation in Budding Yeast

Epigenetic marks such as histone modifications play roles in various chromosome dynamics in mitosis and meiosis. Methylation of histones H3 at positions K4 and K79 is involved in the initiation of recombination and the recombination checkpoint, respectively, during meiosis in the budding yeast. Set1 promotes H3K4 methylation while Dot1 promotes H3K79 methylation. In this study, we carried out detailed analyses of meiosis in mutants of the SET1 and DOT1 genes as well as methylation-defective mutants of histone H3. We confirmed the role of Set1-dependent H3K4 methylation in the formation of double-strand breaks (DSBs) in meiosis for the initiation of meiotic recombination, and we showed the involvement of Dot1 (H3K79 methylation) in DSB formation in the absence of Set1-dependent H3K4 methylation. In addition, we showed that the histone H3K4 methylation-defective mutants are defective in SC elongation, although they seem to have moderate reduction of DSBs. This suggests that high levels of DSBs mediated by histone H3K4 methylation promote SC elongation.     

Ancestral Eukaryotes Reproduced Asexually,Facilitated by Polyploidy: A Hypothesis

The notion that eukaryotes are ancestrally sexual has been gaining attention. This idea comes in part from the discovery of sets of “meiosis‐specific genes” in the genomes of protists. The existence of these genes has persuaded many that these organisms may be engaging in sex, even though this has gone undetected. The involvement of sex in protists is supported by the view that asexual reproduction results in the accumulation of mutations that would inevitably result in the decline and extinction of such lineages. It is argued that this phenomenon can be obviated by polyploidy and that the “meiosis‐specific genes” are used in other processes, including polyploidy control and homologous recombination, independent of meiosis. These phenomena account for the finding that these genes are expressed in cultures devoid of apparent cell fusion events. Hence, it is also proposed that asexual, and not sexual, reproduction is the ancestral condition.     

A phylogenomic inventory of meiotic genes; evidence for sex in Giardia and an early eukaryotic origin of meiosis

Sexual reproduction in eukaryotes is accomplished by meiosis, a complex and specialized process of cell division that results in haploid cells (e.g., gametes). The stereotypical reductive division in meiosis is a major evolutionary innovation in eukaryotic cells, and delineating its history is key to understanding the evolution of sex. Meiosis arose early in eukaryotic evolution, but when and how meiosis arose and whether all eukaryotes have meiosis remain open questions. The known phylogenetic distribution of meiosis comprises plants, animals, fungi, and numerous protists. Diplomonads including Giardia intestinalis (syn. G. lamblia) are not known to have a sexual cycle; these protists may be an early-diverging lineage and could represent a premeiotic stage in eukaryotic evolution. We surveyed the ongoing G. intestinalis genome project data and have identified, verified, and analyzed a core set of putative meiotic genes-including five meiosis-specific genes-that are widely present among sexual eukaryotes. The presence of these genes indicates that: (1) Giardia is capable of meiosis and, thus, sexual reproduction, (2) the evolution of meiosis occurred early in eukaryotic evolution, and (3) the conserved meiotic machinery comprises a large set of genes that encode a variety of component proteins, including those involved in meiotic recombination.     

Local Stressors Reduce Coral Resilience to Bleaching

Coral bleaching, during which corals lose their symbiotic dinoflagellates, typically corresponds with periods of intense heat stress, and appears to be increasing in frequency and geographic extent as the climate warms. A fundamental question in coral reef ecology is whether chronic local stress reduces coral resistance and resilience from episodic stress such as bleaching, or alternatively promotes acclimatization, potentially increasing resistance and resilience. Here we show that following a major bleaching event, Montastraea faveolata coral growth rates at sites with higher local anthropogenic stressors remained suppressed for at least 8 years, while coral growth rates at sites with lower stress recovered in 2–3 years. Instead of promoting acclimatization, our data indicate that background stress reduces coral fitness and resilience to episodic events. We also suggest that reducing chronic stress through local coral reef management efforts may increase coral resilience to global climate change.     

An expanded inventory of conserved meiotic genes provides evidence for sex in Trichomonas vaginalis

Meiosis is a defining feature of eukaryotes but its phylogenetic distribution has not been broadly determined, especially among eukaryotic microorganisms (i.e. protists)-which represent the majority of eukaryotic 'supergroups'. We surveyed genomes of animals, fungi, plants and protists for meiotic genes, focusing on the evolutionarily divergent parasitic protist Trichomonas vaginalis. We identified homologs of 29 components of the meiotic recombination machinery, as well as the synaptonemal and meiotic sister chromatid cohesion complexes. T. vaginalis has orthologs of 27 of 29 meiotic genes, including eight of nine genes that encode meiosis-specific proteins in model organisms. Although meiosis has not been observed in T. vaginalis, our findings suggest it is either currently sexual or a recent asexual, consistent with observed, albeit unusual, sexual cycles in their distant parabasalid relatives, the hypermastigotes. T. vaginalis may use meiotic gene homologs to mediate homologous recombination and genetic exchange. Overall, this expanded inventory of meiotic genes forms a useful "meiosis detection toolkit". Our analyses indicate that these meiotic genes arose, or were already present, early in eukaryotic evolution; thus, the eukaryotic cenancestor contained most or all components of this set and was likely capable of performing meiotic recombination using near-universal meiotic machinery.     

OCCURRENCE OF ENDOSYMBIOTIC BACTERIA IN MARINE DINOFLAGELLATES1,2

The marine dinoflagellates Gymnodinium splendens (photosynthetic) and Cryptothecodinium cohnii (heterotrophic) harbor abundant endosymbiotic bacterial floras. Some general observations are made on their characteristics, and on this symbiotic relationship in other protists.     

Mechanisms of human minisatellite mutation in yeast

Minisatellites are tandem repeat loci, with repeat units ranging in size from 5 bp to 100 bp. The total lengths of repeat arrays vary from about 0.5 kb to 30 kb, and excessive variability in allele length at human minisatellite loci is the result of germline-specific complex recombination events generating new length alleles. Minisatellite alleles also mutate to new lengths in somatic cells, but this occurs at a much lower rate than in the germline. Since recombination is involved in minisatellite mutation, the yeast Saccharomyces cerevisiae is a suitable model organism that has been employed to further dissect the molecular basis of mutation events at human minisatellites. These studies have shown that the mutational behaviour of a minisatellite in meiosis is not determined by the intrinsic properties of the repeat array, but are highly dependent on the position of the minisatellite in the genome. The processes for minisatellite mutation in yeast and humans are identical in the sense that mutation is indeed driven by meiotic recombination, but differ with regard to the types of structural changes that are generated by the recombination events. Tetrad analyses showed that inter-allelic transfers of repeats occur by conversion and not crossing over, and that several chromatids can be involved in successive recombination events in one meiosis, resulting in mutant alleles in several spores. It has been demonstrated that the genes SPO11 and RAD50, involved in the initiation of recombination events, are required for human minisatellite mutation in yeast meiosis. Intrinsic properties of the repeat array appear to determine the stability of human minisatellites in yeast mitosis, since mitotic mutation rates in yeast are highly variable between minisatellites. The repair genes RAD27 and DNA2 stabilise human minisatellites in yeast mitosis, while RAD5 has no effect on mitotic stability. MSH2 depresses human minisatellite frequency in meiotic cells of yeast.     

Molecular characterisation of two paralogous SPO11 homologues in Arabidopsis thaliana

The Spo11 protein of yeast has been found to be covalently bound to double-strand breaks in meiosis, demonstrating a unique role of the protein in the formation of these breaks. Homologues of the SPO11 gene have been found in various eukaryotes, indicating that the machinery involved in meiotic recombination is conserved in eukaryotes. Here we report on SPO11 homologues in plants. In contrast to what is known from other eukaryotes, Arabidopsis thaliana carries in its genome at least two SPO11 homologues, AtSPO11-1 and AtSPO11-2. Both genes are not more closely related to each other than to other eukaryotic SPO11 homologues, indicating that they did not arise via a recent duplication event during higher plant evolution. For both genes three different polyadenylation sites were found. AtSPO11-1 is expressed not only in generative but also to a lesser extent in somatic tissues. We were able to detect in different organs various AtSPO11-1 cDNAs in which introns were differently spliced—a surprising phenomenon also reported for SPO11 homologues in mammals. In the case of AtSPO11-2 we found that the 3′ end of the mRNA is overlapping with a mRNA produced by a gene located in inverse orientation next to it. This points to a possible antisense regulation mechanism. Our findings hint to the intriguing possibility that, at least for plants, Spo11-like proteins might have more and possibly other biological functions than originally anticipated for yeast.     

Multiple Pathways Suppress Non-Allelic Homologous Recombination during Meiosis in Saccharomyces cerevisiae

Recombination during meiosis in the form of crossover events promotes the segregation of homologous chromosomes by providing the only physical linkage between these chromosomes. Recombination occurs not only between allelic sites but also between non-allelic (ectopic) sites. Ectopic recombination is often suppressed to prevent non-productive linkages. In this study, we examined the effects of various mutations in genes involved in meiotic recombination on ectopic recombination during meiosis. RAD24, a DNA damage checkpoint clamp-loader gene, suppressed ectopic recombination in wild type in the same pathway as RAD51. In the absence of RAD24, a meiosis-specific recA homolog, DMC1, suppressed the recombination. Homology search and strand exchange in ectopic recombination occurred when either the RAD51 or the DMC1 recA homolog was absent, but was promoted by RAD52. Unexpectedly, the zip1 mutant, which is defective in chromosome synapsis, showed a decrease, rather than an increase, in ectopic recombination. Our results provide evidence for two types of ectopic recombination: one that occurs in wild-type cells and a second that occurs predominantly when the checkpoint pathway is inactivated.