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

Chi, Jingyun; Parrow, Matthew W.; Dunthorn, Micah

doi:10.1111/jeu.12110

Cited by 74 publications

(80 citation statements)

References 55 publications

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“…These gene sets probably allowed the transition from unicellular organisms to metazoans. Meiosis-associated genes are also found in Symbiodinium (Alveolata), this dinoflagellate probably having sex in its rarely observed free-living state while being asexual in marine symbiosis (51). Finally, wellstudied parasitic protists from highly diverse lineages of amoebozoans, apicomplexans (Alveolata), and kinetoplastids are also giving up their sexual secrets.…”

Section: Sex In Eukaryotic Microorganisms: More Voyeurs Neededmentioning

confidence: 92%

Sex is a ubiquitous, ancient, and inherent attribute of eukaryotic life

Speijer

Lukeš

Eliáš

2015

Proc. Natl. Acad. Sci. U.S.A.

264

267

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Sexual reproduction and clonality in eukaryotes are mostly seen as exclusive, the latter being rather exceptional. This view might be biased by focusing almost exclusively on metazoans. We analyze and discuss reproduction in the context of extant eukaryotic diversity, paying special attention to protists. We present results of phylogenetically extended searches for homologs of two proteins functioning in cell and nuclear fusion, respectively (HAP2 and GEX1), providing indirect evidence for these processes in several eukaryotic lineages where sex has not been observed yet. We argue that (i) the debate on the relative significance of sex and clonality in eukaryotes is confounded by not appropriately distinguishing multicellular and unicellular organisms; (ii) eukaryotic sex is extremely widespread and already present in the last eukaryotic common ancestor; and (iii) the general mode of existence of eukaryotes is best described by clonally propagating cell lines with episodic sex triggered by external or internal clues. However, important questions concern the relative longevity of true clonal species (i.e., species not able to return to sexual procreation anymore). Long-lived clonal species seem strikingly rare. We analyze their properties in the light of meiotic sex development from existing prokaryotic repair mechanisms. Based on these considerations, we speculate that eukaryotic sex likely developed as a cellular survival strategy, possibly in the context of internal reactive oxygen species stress generated by a (proto) mitochondrion. Thus, in the context of the symbiogenic model of eukaryotic origin, sex might directly result from the very evolutionary mode by which eukaryotic cells arose.reactive oxygen species | evolution | protists | eukaryotes | sex

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Section: Sex In Eukaryotic Microorganisms: More Voyeurs Neededmentioning

confidence: 92%

Sex is a ubiquitous, ancient, and inherent attribute of eukaryotic life

Speijer

Lukeš

Eliáš

2015

Proc. Natl. Acad. Sci. U.S.A.

264

267

View full text Add to dashboard Cite

show abstract

“…Now, a suite of hierarchical molecular markers and population genetic data are being used to define precise species boundaries and refine Symbiodinium taxonomy (LaJeunesse et al, 2012, 2014; Jeong et al, 2014). Though it has yet to be physically observed, overwhelming molecular evidence indicates that Symbiodinium engage in sex at some frequency in the wild, either within the coral habitat or in the external environment (Baillie et al, 2000; LaJeunesse, 2001; Santos et al, 2004; Sampayo et al, 2009; Pettay et al, 2011; Baums et al, 2014; Chi et al, 2014; Thornhill et al, 2014). Sympatric symbionts found in distinct colonies of the same host species in the same environments exhibit diagnostic microsatellite allele frequencies, revealing genetic recombination within but not between groups (LaJeunesse et al, 2014).…”

Section: Defining Coral–algal Diversitymentioning

confidence: 99%

The extended phenotypes of marine symbioses: ecological and evolutionary consequences of intraspecific genetic diversity in coralâ€“algal associations

2014

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Reef-building corals owe much of their success to a symbiosis with dinoflagellate microalgae in the genus Symbiodinium. In this association, the performance of each organism is tied to that of its partner, and together the partners form a holobiont that can be subject to selection. Climate change affects coral reefs, which are declining globally as a result. Yet the extent to which coral holobionts will be able to acclimate or evolve to handle climate change and other stressors remains unclear. Selection acts on individuals and evidence from terrestrial systems demonstrates that intraspecific genetic diversity plays a significant role in symbiosis ecology and evolution. However, we have a limited understanding of the effects of such diversity in corals. As molecular methods have advanced, so too has our recognition of the taxonomic and functional diversity of holobiont partners. Resolving the major components of the holobiont to the level of the individual will help us assess the importance of intraspecific diversity and partner interactions in coral–algal symbioses. Here, we hypothesize that unique combinations of coral and algal individuals yield functional diversity that affects not only the ecology and evolution of the coral holobiont, but associated communities as well. Our synthesis is derived from reviewing existing evidence and presenting novel data. By incorporating the effects of holobiont extended phenotypes into predictive models, we may refine our understanding of the evolutionary trajectory of corals and reef communities responding to climate change.

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“…Consequently, several studies have successfully documented full complements of meiotic genes in diverse putative asexual microbes including some ciliates (e.g., Ichthyophthirius multifiliis ) (Chi et al. 2014a), dinoflagellates (Chi et al. 2014b), fungi, diplomonads, and amoebae (Malik et al.…”

Section: Introductionmentioning

confidence: 99%

Amoebozoans are Secretly but Ancestrally Sexual: Evidence for Sex Genes and Potential Novel Crossover Pathways in Diverse Groups of Amoebae

et al. 2017

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Sex is beneficial in eukaryotes as it can increase genetic diversity, reshuffle their genomes, and purge deleterious mutations. Yet, its evolution remains a mystery. The eukaryotic clade supergroup Amoebozoa encompasses diverse lineages of polymorphic amoeboid forms, including both free-living and parasitic lineages. The group is generally believed to be asexual, though recent studies show that some of its members are implicated in cryptic forms of sexual cycles. In this study, we conduct a comprehensive inventory and analysis of genes involved in meiosis and related processes, in order to investigate the evolutionary history of sex in the clade. We analyzed genomic and transcriptomic data of 39 amoebozoans representing all major subclades of Amoebozoa. Our results show that Amoebozoa possess most of the genes exclusive to meiosis but lack genes encoding synaptonemal complex (SC). The absence of SC genes is discussed in the context of earlier studies that reported ultrastructural evidence of SC in some amoebae. We also find interclade and intrageneric variation in sex gene distribution, indicating diversity in sexual pathways in the group. Particularly, members of Mycetozoa engage in a novel sexual pathway independent of the universally conserved meiosis initiator gene, SPO11. Our findings strongly suggest that not only do amoebozoans possess sex genes in their genomes, but also, based on the transcriptome evidence, the present sex genes are functional. We conclude that Amoebozoa is ancestrally sexual, contrary to the long held belief that most of its members are asexual. Thus, asexuality in Amoebozoa, if confirmed to be present, is a derived-trait that appeared later in their evolution.

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

Cited by 74 publications

References 55 publications

Sex is a ubiquitous, ancient, and inherent attribute of eukaryotic life

Sex is a ubiquitous, ancient, and inherent attribute of eukaryotic life

The extended phenotypes of marine symbioses: ecological and evolutionary consequences of intraspecific genetic diversity in coralâ€“algal associations

Amoebozoans are Secretly but Ancestrally Sexual: Evidence for Sex Genes and Potential Novel Crossover Pathways in Diverse Groups of Amoebae

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