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Abstract
Recognizing the life cycle of an organism is key to understanding its biology and ecological impact. Emiliania huxleyi is a cosmopolitan marine microalga, which displays a poorly understood biphasic sexual life cycle comprised of a calcified diploid phase and a morphologically distinct biflagellate haploid phase. Diploid cells (2N) form large-scale blooms in the oceans, which are routinely terminated by specific lytic viruses (EhV). In contrast, haploid cells (1N) are resistant to EhV. Further evidence indicates that 1N cells may be produced during viral infection. A shift in morphology, driven by meiosis, could therefore constitute a mechanism for E. huxleyi cells to escape from EhV during blooms. This process has been metaphorically coined the ‘Cheshire Cat’ (CC) strategy. We tested this model in two E. huxleyi strains using a detailed assessment of morphological and ploidy-level variations as well as expression of gene markers for meiosis and the flagellate phenotype. We showed that following the CC model, production of resistant cells was triggered during infection. This led to the rise of a new subpopulation of cells in the two strains that morphologically resembled haploid cells and were resistant to EhV. However, ploidy-level analyses indicated that the new resistant cells were diploid or aneuploid. Thus, the CC strategy in E. huxleyi appears to be a life-phase switch mechanism involving morphological remodeling that is decoupled from meiosis. Our results highlight the adaptive significance of morphological plasticity mediating complex host–virus interactions in marine phytoplankton.
Highlights
The life cycle of an organism represents a multitude of cellular stages connected by reproductive processes
To investigate the molecular mechanisms underlying the Cheshire Cat’ (CC) strategy, we monitored the interplay between lytic virus E. huxleyi viruses (EhV)-201 [16] and two E. huxleyi strains: RCC 1216, a 2N calcified strain able to undergo sexual transitions and form biflagellate 1N cells [8]; and CCMP 2090, a 2N noncalcified strain, lacking essential flagellar genes and for which the production of 1N cells has never been recorded [15]
During viral infection of RCC 1216 (Fig 1A–1I), there was a transient rise in noncalcified cells between 2 and 4 days postinfection
Summary
The life cycle of an organism represents a multitude of cellular stages connected by reproductive processes. With the exception of a few model organisms and human parasites, little is known about the life cycle of microbial eukaryotes, which paradoxically represent the vast majority of extant eukaryotic diversity [3] This knowledge gap is exemplified by marine phytoplankton, which comprise a highly diverse assemblage of phototrophic species that make an important contribution to the base of the marine food web and global biogeochemical processes [2,4]. 1N cells have been denoted scale-bearing swarmers or ‘S-cells’ [7] Both 2N and 1N cells can grow independently by mitosis and likely interconnect through sex and meiosis, sexual reproduction has never been observed in E. huxleyi
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