Effects of Nutrient Limitation on the Synthesis of N-Rich Phytoplankton Toxins: A Meta-Analysis

Abstract

Eutrophication has played a major role in the worldwide increase of harmful algal blooms (HABs). Higher input of key nutrients, such as nitrogen (N) and phosphorus (P), can stimulate the growth of harmful algal species in freshwater, estuarine, and coastal marine ecosystems. Some HAB-forming taxa, particularly several cyanobacteria and dinoflagellate species, are harmful through the production of N-rich toxins that have detrimental effects on the environment and human health. Here, we test how changes in nutrient availability affect N-rich toxin synthesis in cyanobacteria and dinoflagellates using a meta-analysis approach. Overall, N-rich toxin content showed an increase with P limitation, while it tended to decrease with N limitation, but we also observed substantial variation in responses both within and across genera and toxin groups. For instance, in response to N limitation, microcystin content varied from a 297% decrease up to a 273% increase, and paralytic shellfish poisoning (PSP) toxin content varied from a 204% decrease to an 82% increase. Cylindrospermopsin, produced by N2-fixing cyanobacteria, showed no clear direction in response to nutrient limitation, and cellular contents of this compound may thus vary independently of nutrient fluctuations. Our results confirm earlier reported stoichiometric regulation of N-rich phytoplankton toxins, showing increased toxin content with an increase in cellular N:P ratios, and vice versa. Thus, changes in N-rich toxin content largely follow the changes in relative cellular N content. Consequently, although nutrient limitation may limit bloom biomass and thereby bloom toxicity, our results warn that P limitation can cause accumulation of cellular toxins and thus lead to unexpected increases in bloom toxicity.

Ecological stoichiometry of functional traits in a colonial harmful cyanobacterium

“…Besides gas vesicles and pigments, other N‐rich traits in phytoplankton have been reported following cellular elemental stoichiometry as well. For example, the synthesis of N‐rich toxic secondary metabolites (e.g., microcystins) was shown to generally decrease upon N limitation and increase under P limitation, thus decreasing with cellular C : N ratio (Van de Waal et al 2009; Gobler et al 2016; Wagner et al 2019; Brandenburg et al 2020).…”

What Colin Reynolds could tell us about nutrient limitation, N:P ratios and eutrophication control

“…Furthermore, the concentration of microcystins (cyanobacterial peptide toxins) in cyanobacterial cells has been proposed to relate to excess availability of nitrogen (e.g. Gobler et al, 2016;Wagner et al, 2019;Brandenburg et al, 2020), and this intuitively seems to be expected on the basis of the high N content of these molecules. However, the opposite has also been observed: experiments addressing the impact of N-limitation (and other growth conditions) on culture strains of various cyanobacteria have shown contradictory results, some of which may have methodological causes.…”

“…Therefore, meaningful results from experiments addressing the impact of N-limitation on the production of microcystins will need to include the production of the totality of oligopeptides. More importantly, the overall outcome of such experiments is that the impact of growth conditions on the microcystin production of a strain is in the range of not more than a factor of 2-4, while the key driver of microcystin concentrations in field populations is the biomass of producing species and clones (for overviews see Fastner & Humpage, in press, and the metaanalysis by Brandenburg et al, 2020). It follows that conditions favouring cyanobacterial dominance and blooms are the more relevant aspect to address.…”

Algal Toxic Compounds and Their Aeroterrestrial, Airborne and other Extremophilic Producers with Attention to Soil and Plant Contamination: A Review

“…Regarding the nutrient availability, most research aimed at the role of key nutrients, such as nitrogen (N) and phosphorus (P), because of the worldwide acceptance that eutrophication has a major role in the increase of harmful algal blooms in freshwater, estuarine, and coastal marine ecosystems. A recent study based on meta-analysis approach showed that overall, N-rich toxin content in cyanoprokaryotes and dinoflagellate increased with P limitation, while it tended to decrease with N limitation [ 124 ]. Although the paleolimnological data on phycotoxins are quite scarce, similar results were obtained on correlation between N and P and MC content in sediments [ 99 ].…”