Imagine a typical dreary day at the Scheldt estuary in The Netherlands. The weak springtime sun paints the exposed tidal plains in a dull brownish hue. However, unbeknownst to the casual observer, the sediment surface of the mudflat is teeming with microscopic life. This so-called “secret garden”  typically takes the form of complex multi-layered biofilms, where microalgae coexist with heterotrophic bacteria . Such phototrophic biofilms are very efficient in their use of solar energy and provide important ecosystem services such as erosion resistance and nutrient cycling . Marine biofilms are in many cases dominated by benthic diatoms , which are far more species-rich compared to planktonic diatoms . Nevertheless, laboratory studies of diatoms have mostly focussed on planktonic diatoms. To counter this, my favorite benthic diatom Seminavis robusta was introduced as a new experimental model organism to help us understand diatom life cycles and adaptation to a benthic habitat .
S. robusta first came on the scene 20 years ago, when it received its current name and the first investigation of its sexual reproduction stages took place [7,8] (Fig. 1). The species inhabits soft sediments and rock surfaces of coastal lagoons in the Northern hemisphere [6,7,9,10]. The experimental toolkit of S. robusta is extensive, comprising cryopreservation , experimental assays to test the effects of sex pheromones [12,13], chemical synthesis of the attraction pheromone diproline [12,14], a culture collection hosting >100 strains , procedures to sexually cross compatible cultures [8,9] and movement-tracking methods to study chemotaxis [15,16]. To complement this, we recently constructed a reference genome for S. robusta containing more than 36,000 protein-coding genes, the largest number found in any diatom so far ! Altogether, these tools spurred research into diverse facets of S. robusta’s benthic lifestyle, such as mate finding, cell migration and interactions with associated bacteria (Fig. 1).
Figure 1: timeline of research on the benthic diatom S. robusta. Live cells are pictured. S. robusta’s valve length ranges from ~70µm (initial cells) to ~15µm (smallest viable cell).
A key feature of diatoms is their size-dependent sexual life cycle. During consecutive mitotic (asexual) divisions, the average cell size of populations diminishes below a sexual size threshold, only to be restored by the formation of an auxospore during sexual reproduction (Fig. 2). Several sexual species are being used to study the life cycle in the laboratory: Pseudo-nitzschia multistriata [18–20], Skeletonema marinoi , Pseudostaurosira trainorii  and, of course, S. robusta.
At the onset of the new year, I want to take a moment to reflect on what we learned about S. robusta’s life cycle in 2021 (Fig. 2): (1) In a series of elegant experiments, Bulankova and colleagues showed that recombination during mitosis is remarkably common . This finding may have important implications for researchers that use established strains, because their genomes gradually diverge from the original isolates. (2) A day/night RNA sequencing experiment revealed that almost all S. robusta genes display rhythmic expression and that the cell cycle was strongly synchronized to the photoperiod . Several peculiar characteristics of the day/night transcriptome were discovered that may prove to be adaptations to the challenges of the benthic environment, such as fluctuations in light and temperature, tidal cycles and rhythmic migration [17,24]. (3) We showed that light conditions have a profound impact on sexual reproduction of S. robusta. Indeed, exposing cultures to low intensity light in the blue spectrum massively boosted the formation of auxospores . (4) Assessing cells’ sensitivity to analogs of the attraction pheromone diproline, Bonneure and colleagues built a proof of concept for diazirine and azide labeling of diproline, opening corridors to identify the diproline receptor . (5) Finally, we compared gene expression between the two mating types (sexes) of S. robusta after treatment with sex inducing pheromones . These pheromones typically result in a cell cycle arrest and cause the start of diproline production, which was reflected in specific gene expression patterns (Fig. 2).
Figure 2. New clues about S. robusta’s life history in the year 2021. Sources: [14,23–26]
On the whole, it is clear that S. robusta played an important role in our current understanding of the lifestyle of benthic diatoms. Nevertheless, the diatom life cycle remains poorly understood from a molecular point of view. One of the greatest remaining mysteries is certainly the mechanism used by cells to measure their own size, which allows them to become sexual only when they become small enough. Furthermore, there are remarkably few microscopic observations of sexual reproduction in the wild. Hence, the timing and geography of diatom sexual reproduction in nature is an area where a lot of progress can be made. To this end, experimental data on the factors that determine the balance between growth and sex is needed to fully understand natural diatom life cycles. Given these fundamental questions, I am very excited to see what S. robusta will teach us in the next 20 years!
Gust Bilcke is a postdoctoral researcher at Ghent University (Belgium). He is fascinated by the genetic and genomic programs behind the diversity in life cycle strategies of diatoms, in particular sexual reproduction and diurnal/circadian rhythms. You can email Gust at Gust.Bilcke[at]psb.vib-ugent.be or leave a message in the comments section if you have any question about the blog post.
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