Trade-off between sex and growth in diatoms: Molecular mechanisms and demographic implications

Annunziata, Rossella; Mele, Bruno Hay; Marotta, Pina; Volpe, Massimiliano; Entrambasaguas, Laura; Mager, Svenja; Stec, Krzysztof; d’Alcalà, Maurizio Ribera; Sanges, Remo; Finazzi, Guido; Iudicone, Daniele; Montresor, Marina; Ferrante, Maria Immacolata

doi:10.1126/sciadv.abj9466

Cited by 15 publications

(15 citation statements)

References 82 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…However, our investigations show that the size reduction period is commonly followed by a period of size homeostasis in which diatoms are able to maintain their cell size within a small range. Thus, timing of the sexual cycle and corresponding leap in cell size, appears to be predominantly triggered by environmental changes or encounters with potential mates, as is the case for other unicellular organisms (Moeys et al ., 2016; Annunziata et al ., 2022).…”

Section: Discussionmentioning

confidence: 99%

Decoupling cell size homeostasis in diatoms from the geometrical constraints of the silica cell-wall

Haan

Ramos

Gal

2023

Preprint

View full text Add to dashboard Cite

Unicellular organisms are known to exert tight control over their cell size. In the case of diatoms, abundant eukaryotic microalgae, the layout of the rigid silica cell wall imposes geometrical restrictions on cell size. A generally accepted theory states that the need to fit any new silica element into a previously formed structure causes a reduction in size with each vegetative division cycle, until cell size restoration is achieved by a switch to another life-cycle stage. Nevertheless, several reported exceptions cast doubt on the generality of this theory. Here, we monitored clonal cultures of the diatom Stephanopyxis turris for up to two years, recording the sizes of thousands of cells, in order to follow the distribution of cell sizes in the population. Our results show that all S. turris cultures above a certain size threshold undergo a gradual size reduction, in accordance with the postulated geometrical driving force. However, once the cell size reaches a lower threshold, a constant size range is maintained by different cellular strategies. These observations suggest two distinct mechanisms to regulate the cell size of diatoms, reduction and homeostasis. The interplay between these mechanisms can explain the behavior of different diatoms species in various environments.

show abstract

Section: Discussionmentioning

confidence: 99%

Decoupling cell size homeostasis in diatoms from the geometrical constraints of the silica cell-wall

Haan

Ramos

Gal

2023

Preprint

View full text Add to dashboard Cite

show abstract

“…RNA quantity was determined using a Qubit 2.0 Fluorometer (Life Technologies, Thermo Fisher Scientific, Waltham, MA, USA) and integrity using a 2100 Bioanalyzer System (Agilent Technologies, Santa Clara, CA, USA). RNA-seq library preparation and sequencing libraries for two samples ( Table S1 ) were performed at the Genecore Facility of the European Molecular Biology Laboratory (EMBL) in Germany as described in Annunziata et al 2022 . Raw data are available in ArrayExpress with accession number E-MTAB-12676.…”

Section: Methodsmentioning

confidence: 99%

DNA methylation is linked to the monoallelic expression ofMRP3, a diatom mating type determining gene

Ruggiero,

Mager,

Manfellotto

et al. 2023

Preprint

Self Cite

View full text Add to dashboard Cite

Diatoms are unicellular microalgae widely distributed in aquatic ecosystems. In diatoms, sexual reproduction is needed to counteract cell miniaturization imposed by the rigid silica shell, and only small cells, below a species-specific size threshold, are competent for sex. We performed a genome-wide Enzymatic Methyl-seq analysis in the heterothallic diatom Pseudo-nitzschia multistriata comparing cells of different size and opposite mating type (MT) to investigate potential epigenetic controls in life cycle transitions. We found an imprinting-like pattern of methylation at the sex locus: alleles of the gene responsible for the specification of the MT+, MRP3, are hypermethylated in MT- and differentially methylated in MT+, with transcription occurring only on the MT+ hypomethylated variant. The methylation pattern is overall stable over the P. multistriata life cycle. Absence of methylation in MRP3 is necessary for its expression but not sufficient, since large non-sexual cells have the same methylation profile of small sexual cells but do not express MRP3, suggesting that additional controls are involved in the mechanism of sex determination.

show abstract

“…These data were recently integrated by a second study focused on gene expression changes during the whole span of the sexual phase (Annunziata et al, 2022). The entire cell population in the cross is arrested in G1 even if only up to 20% of the cells will eventually undergo meiosis.…”

Section: A Model For Se Xual Reproductionmentioning

confidence: 99%

“…Ferrante, unpublished). Annunziata et al (2022) also explored the ecological implication of the growth arrest during sexual reproduction with a model showing that the parental growth arrest impacts the F1 cell cohort size.…”

Section: A Model For Se Xual Reproductionmentioning

confidence: 99%

“…The presence of multiple functional cell types in a seemingly identical cell population in the cross has been recently confirmed using single nuclei RNA‐seq (M. I. Ferrante, unpublished). Annunziata et al (2022) also explored the ecological implication of the growth arrest during sexual reproduction with a model showing that the parental growth arrest impacts the F1 cell cohort size.…”

Section: A Model For Sexual Reproductionmentioning

confidence: 99%

See 1 more Smart Citation

The pennate diatom Pseudo‐nitzschia multistriata as a model for diatom life cycles, from the laboratory to the sea

Ferrante

Broccoli

Montresor

2023

Journal of Phycology

Self Cite

View full text Add to dashboard Cite

Phytoplankton dynamics are regulated by external cues, such as light and nutrients, as well as by biotic interactions and endogenous controls linked to life cycle characteristics. The planktonic pennate diatom Pseudo‐nitzschia multistriata, with a heterothallic mating system with two opposite mating types (MTs), represents a model for the study of diatom life cycles. P. multistriata is a toxic species, able to produce the neurotoxin domoic acid. First described in Japan in 1993, it was detected at the long‐term monitoring station MareChiara (Gulf of Naples, Italy) in 1995. Since then, P. multistriata has been reported from several worldwide coastal sites. A large body of knowledge has been produced on its ecology, genetic diversity, and life cycle characteristics. The availability of these data, the ecological relevance of the Pseudo‐nitzschia genus, and its controllable life cycle with a short generation time made it an ideal species to develop a genetic model system for diatoms. To enable functional studies, a 59 Mb genome sequence and several transcriptomic data were produced, and genetic transformation was optimized. These tools allowed the discovery of the first mating‐type determining gene for diatoms. Gene expression studies and metabolomics analyses defined genes and molecules underpinning different phases of the process of sexual reproduction. This model system, developed to explore the genetics of diatom life cycles, offers the opportunity to parallel experimental observations in the laboratory using in situ meta‐omics analyses along space and time, empowering knowledge on the biology and ecology of the genus.

show abstract

Trade-off between sex and growth in diatoms: Molecular mechanisms and demographic implications

Cited by 15 publications

References 82 publications

Decoupling cell size homeostasis in diatoms from the geometrical constraints of the silica cell-wall

Decoupling cell size homeostasis in diatoms from the geometrical constraints of the silica cell-wall

DNA methylation is linked to the monoallelic expression ofMRP3, a diatom mating type determining gene

The pennate diatom Pseudo‐nitzschia multistriata as a model for diatom life cycles, from the laboratory to the sea

Contact Info

Product

Resources

About