Thoughts on the evolution and ecological niche of diatoms

Abstract

Diatoms are the most recent major algal lineage added to the geological record, appearing more than 200 million years ago. They are stramenopile protists resulting from a secondary endosymbiotic event that yielded the only photosynthetic protistan lineage expressing external siliceous cell wall structures called frustules. Many diatoms also have large internal vacuoles and a common assumption in the literature is that success of the diatoms is largely attributable to these two morphological inventions: the frustule for defense and vacuole for luxury nutrient uptake. Here, we revisit the evolution of these inventions, propose sequential steps in frustule development, replace luxury nutrient uptake with predator defense and buoyancy control as the driver of vacuole expansion, and suggest that perhaps the greatest significance of the frustule for diatom evolution is the secondary consequence of enhancing sexual reproduction. In this synthesis, we emphasize a distinction between the 'general' success of diatoms and the success of 'bloom-forming' species, as the physiological and morphological drivers of these successes differ. Importantly, the bloom-forming species are responsible for the major role of diatoms in aquatic biogeochemical cycles. The bloom-forming habit we ascribe to specific physiological attributes that, at their core, revolve around influencing the balance between diatom growth and losses to predators. We propose that these physiological adaptations are linked to size-dependent maximum division rates in bloom-forming diatoms, due to size-scaling of predator-prey interactions. The existence of these bloom-forming species yields an apparent allometric relationship that has previously been interpreted in terms of nutrient acquisition.Our analysis yields insights into species successions during blooms, considers the fundamental benefit of blooming (and subsequent sinking) from a reproductive standpoint, and provides some reinterpretation of diatoms success over geologic time and in the modern ocean.

Predatory cues drive colony size reduction in marine diatoms

“…In the microscopic marine environment, colony formation in phytoplankton is very common, especially in cyanobacteria, green algae, dinoflagellates, and diatoms (Hessen & Van Donk, 1993;Rippka et al, 1979;Smayda, 2010). Diatoms are one of the largest groups of phytoplankton, often forming long chains which plays a significant role in the cycling of oxygen and carbon from the earth's atmosphere (Behrenfeld, 2021).…”

“…Diatom carbon fixation consequently equals the total carbon emissions from fossil fuels, ~10 Gt C y −1 (Le Quéré et al, 2015;Longhurst et al, 1995). In the marine environment, it has been estimated that diatoms supply up to 45% of the total primary production (Mann, 1999), and they flourish in aquatic environments by making the most from their vacuoles, buoyancy regulation, and luxury nutrient uptake (Behrenfeld, 2021;Hansen & Visser, 2019). Chain formation is one of the more conspicuous traits they possess and is speculated to be driven by predation, although this is still debated (Behrenfeld, 2021;Verity & Villareal, 1986; Figure 1).…”

“…In the marine environment, it has been estimated that diatoms supply up to 45% of the total primary production (Mann, 1999), and they flourish in aquatic environments by making the most from their vacuoles, buoyancy regulation, and luxury nutrient uptake (Behrenfeld, 2021;Hansen & Visser, 2019). Chain formation is one of the more conspicuous traits they possess and is speculated to be driven by predation, although this is still debated (Behrenfeld, 2021;Verity & Villareal, 1986; Figure 1). Chains are typically formed with silica or chitin strands between daughter cells, accompanied by mitotic division (Round et al, 1990;Young et al, 2012).…”

Editorial: Unraveling Mechanisms Underlying Annual Plankton Blooms in the North Atlantic and Their Implications for Biogenic Aerosol Properties and Cloud Formation

“…The NAAMES experience also yielded a variety of higherlevel syntheses regarding phytoplankton bloom hypotheses (Behrenfeld and Boss, 2018), diatom ecology and evolution (Behrenfeld et al, 2021a), phytoplankton size distributions and succession (Behrenfeld et al, 2021c), and a new interpretation of Hutchinson's (1961) "Paradox of the Plankton" regarding the unexpected diversity of phytoplankton species in water columns with few readily identifiable niches (Behrenfeld et al, 2021b).…”

Protoplasmic streaming of chloroplasts enables rapid photoacclimation in large diatoms

“…For those that graze on these large diatoms, their lowered gC: cell-volume also makes them a lower-value food package than similarly sized other plankton (McBeain and Halsey, 2018). In addition, a new hypothesis proposes that a niche for large diatoms exists because of the non-static dynamics of the predator-prey ratio (Behrenfeld et al, 2021a(Behrenfeld et al, , 2021b; the existence of some lag time before the appearance of an adequatesized predator allows large diatoms to grow intensively. It is also likely that large-celled phytoplankton are relatively less susceptible to virus attack because although larger cells are more likely to encounter viruses, the decreased cell abundance provides insufficient hosts to support high rates of virus attack (Flynn et al, 2021).…”