Life-cycle modification in open oceans accounts for genome variability in a cosmopolitan phytoplankton

Dassow, Peter von; John, Uwe; Ogata, Hiroyuki; Probert, Ian; Bendif, El Mahdi; Kegel, Jessica; Audic, Stéphane; Wincker, Patrick; Silva, Corinne Da; Claverie, Jean‐Michel; Doney, Scott C.; Glover, David M.; Flores, Daniella Mella; Herrera, Yeritza; Lescot, Magali; Garet-Delmas, Marie José; Vargas, Colomban de

doi:10.1038/ismej.2014.221

Cited by 71 publications

(79 citation statements)

References 58 publications

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“…Amphimedon queenslandica ). The presence of only three fragmented dynein genes in Emiliania huxleyi was attributed to the loss of most flagellar genes in the sequenced strain and is not a characteristic of the species itself (von Dassow et al 2015). Thus, given the deep taxonomic sampling of this study, loosing a single axonemal dynein is a rare event.…”

Section: Resultsmentioning

confidence: 99%

Fine-Tuning Motile Cilia and Flagella: Evolution of the Dynein Motor Proteins from Plants to Humans at High Resolution

Kollmar

2016

Mol Biol Evol

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The flagellum is a key innovation linked to eukaryogenesis. It provides motility by regulated cycles of bending and bend propagation, which are thought to be controlled by a complex arrangement of seven distinct dyneins in repeated patterns of outer- (OAD) and inner-arm dynein (IAD) complexes. Electron tomography showed high similarity of this axonemal repeat pattern across ciliates, algae, and animals, but the diversity of dynein sequences across the eukaryotes has not yet comprehensively been resolved and correlated with structural data. To shed light on the evolution of the axoneme I performed an exhaustive analysis of dyneins using the available sequenced genome data. Evidence from motor domain phylogeny allowed expanding the current set of nine dynein subtypes by eight additional isoforms with, however, restricted taxonomic distributions. I confirmed the presence of the nine dyneins in all eukaryotic super-groups indicating their origin predating the last eukaryotic common ancestor. The comparison of the N-terminal tail domains revealed a most likely axonemal dynein origin of the new classes, a group of chimeric dyneins in plants/algae and Stramenopiles, and the unique domain architecture and origin of the outermost OADs present in green algae and ciliates but not animals. The correlation of sequence and structural data suggests the single-headed class-8 and class-9 dyneins to localize to the distal end of the axonemal repeat and the class-7 dyneins filling the region up to the proximal heterodimeric IAD. Tracing dynein gene duplications across the eukaryotes indicated ongoing diversification and fine-tuning of flagellar functions in extant taxa and species.

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Section: Resultsmentioning

confidence: 99%

Fine-Tuning Motile Cilia and Flagella: Evolution of the Dynein Motor Proteins from Plants to Humans at High Resolution

Kollmar

2016

Mol Biol Evol

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“…Remarkably, diploid-haploid switching is triggered by sensing specific E. huxleyi viruses (EhVs) that infect and destroy diploid, but not haploid cells (61). However, genomic evidence suggests that putative asexual lineages of E. huxleyi that lost the ability to switch to the haploid stage have recurrently emerged in populations inhabiting oligotrophic open oceans, perhaps as a consequence of low levels of EhVs in these environments (62).…”

Section: Sex In Eukaryotic Microorganisms: More Voyeurs Neededmentioning

confidence: 99%

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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“…But the exact cause of differential survival between coastal and oceanic taxa is still not known. Further, von Dassow et al () showed that coastal, highly productive, and seasonally cycling parts were populated with Emiliania huxleyi strains maintaining the biphasic life‐cycle, while a loss of flagella and 1N phase occurred in some open ocean sub‐populations of E. huxleyi . von Dassow et al () speculate that this loss of the haploid phase could be related to lower biotic pressure and low environmental variability of the ocean, as opposed to highly variable environmental conditions of neritic environments that favor sexuality (von Dassow et al ).…”

mentioning

confidence: 99%

Coastal zones as important habitats of coccolithophores: A study of species diversity, succession, and life‐cycle phases

Godrijan

Young

Pfannkuchen

et al. 2018

Limnology & Oceanography

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Coccolithophores are unicellular calcifying eukaryotes with a complex life‐cycle; they are important primary producers, and major drivers of global biogeochemical cycles. The majority of research on coccolithophores has been focused on open ocean waters, while the knowledge of their roles in coastal ecosystems is limited. Early 20th century studies of the Adriatic coast produced major taxonomic papers describing half of the projected diversity of coccolithophores. Afterwards, there have been only scarce records of their diversity and ecology in the Adriatic, and coastal systems in general. We aimed to assess coccolithophore diversity and species succession, and closely examine their ecological preferences in the coastal area of the northern Adriatic. We recorded coccolithophores throughout the year at 100% frequency, documented 52 taxa, abundances as high as 2.4 × 105 cells L−1, and noted the winter domination over the phytoplankton community. Out of 52 observed coccolithophore taxa, 31 were heterococcolithophorids and 21 holococcolithophorids. Moreover, seven pairs of heterococcolith and holococcolith phases were noted, and two strategies of temporal separation of life‐cycle phases were observed. We report ecological preferences of those life‐cycle pairs and give in situ evidence that holo‐ and heterococcolith phases are widening the specie's ecological niches. This expansion allows the species to exploit a wider range of ecological conditions and enables phenotypic plasticity, important in response to changes in the environment. With this study we emphasize that coastal areas are highly productive for coccolithophore studies. Our results indicate that a shift in research effort on coccolithophores in the coastal waters is needed.

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Life-cycle modification in open oceans accounts for genome variability in a cosmopolitan phytoplankton

Cited by 71 publications

References 58 publications

Fine-Tuning Motile Cilia and Flagella: Evolution of the Dynein Motor Proteins from Plants to Humans at High Resolution

Fine-Tuning Motile Cilia and Flagella: Evolution of the Dynein Motor Proteins from Plants to Humans at High Resolution

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

Coastal zones as important habitats of coccolithophores: A study of species diversity, succession, and life‐cycle phases

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