The twelfth Tansley Lecture. Small is beautiful: the picophytoplankton

1. Picophytoplankton are planktonic photosynthetic O2-evolvers that can pass through 2 μm-diameter pores; they include prokaryotic (eubacterial) and eukaryotic members and occur in freshwater and marine habitats. There are no photosynthetic reproductive and dispersal stages of benthic macrophytes of picoplanktonic size. The picophytoplankton condition appears to be derived and polyphyletic in both prokaryotes and eukaryotes. 2. Picophytoplankton are among the smallest free-living cells, despite having to contain the photosynthetic apparatus, which occupies about half of the cell volume, as well as core cellular machinery. The size of the smallest prokaryotic (0·6 μm diameter) and eukaryotic (0·95 μm diameter) picophytoplankton are close to the minimum possible size estimated from the occurrence of non-scalable essential components such as the genome and plasmalemma and other membranes. 3. Picophytoplankton cells have advantages relative to larger phytoplankton cells in terms of resource acquisition and the subsequent use of the resources in catalysing cell growth and reproduction. The smaller package effect in light harvesting means smaller resource (energy, C, N, Fe, Mn, Cu) costs of photon harvesting and transformation into chemical energy in small than in large cells. The smaller diffusion boundary layer around small cells, coupled with smaller nutrient fluxes per unit plasmalemma area needed to attain a given fraction of the maximum specific growth rate in smaller cells, increases the availability of low concentrations of nutrients to small relative to larger cells. If the supply of CO2 to the core photosynthetic carboxylase ribulose bisphosphate carboxylase-oxygenase is purely by diffusion then smaller cells could satisfy their catalytic requirements with less of this enzyme whose synthesis has high energy, C and N costs. Overall, resources can be acquired, and used in growth, more effectively in smaller than in larger cells. 4. Some factors work against the conclusion in (3.) but, in most habitats, do not negate these conclusions. Examples related to non-scalable essential cell components are the use of energy, C, N and P in the genome and of energy, C, N, P and Fe in the plasma membrane. Transport-related factors include the increased potential cell volume-specific leakage of accumulated resources, and the greater cell volume-specific energy costs of motility at a given speed, in smaller than in larger cells. The smaller package effect in smaller cells involves a greater potential for photodamage by both photosynthetically active radiation and by UV-B. 5. Picophytoplankton occurrence is also a function of factors which lead to cell loss. Factors such as sinking out of the euphotic zone and parasitism by eukaryotes such as chytrids are less significant for picophytoplankton than for larger cells, whereas viral parasitism and grazing by appropriately sized grazers are likely to be at least as great for picophytoplankton as for larger cells. 6. The totality of the effects mentioned in (3.) above suggests that picophytoplankton should generally have higher specific growth rates (probably) in resource-saturated (photons, C, N, P, Fe, etc.) and (certainly) in resource-limited environments than do larger cells. The distribution of picophytoplankton is certainly consistent with their ability to capitalize on resource-limited environments: they contribute a larger fraction of biomass and productivity relative to larger cells in low-nutrient than in high-nutrient environments, and in low-light (e.g. the deep chlorophyll maximum) than in high-light environments. 7. Sexual reproduction is apparently rare in picophytoplankton, with implications for species definition. There are probably relatively few species (hundreds or thousands) with very wide biogeographical ranges in marine or in freshwater habitats. The small size and (probably) low biodiversity means large numbers of individuals worldwide, e.g. c.1026 individuals of the commonest species of the marine cyanobacterium Synechococcus. Picophytoplankton contribute at least one-tenth (i.e. in excess of 3 Pg C per year) to global aquatic net primary productivity.