Ecological stoichiometry of functional traits in a colonial harmful cyanobacterium

Abstract

Trait-based approaches provide a mechanistic framework crossing scales from cellular traits to community dynamics, while ecological stoichiometry applies first principles to understand how the balance of energy and elements shape ecological interactions. However, few studies have explicitly linked both frameworks. In this study, we tested the stoichiometric regulation of a number of carbon (C) based (e.g., extracellular polysaccharides and colony formation) and nitrogen (N) containing traits (i.e., chlorophyll a, phycocyanin, and gas vesicle content) in cyanobacteria in laboratory experiments and in the field. We exposed the cosmopolitan colony forming freshwater cyanobacterium Microcystis sp. in batch experiments to light, N and phosphorus (P) limitation, and enhanced CO 2 levels, and assessed the regulation of these traits. Cyanobacterial traits followed stoichiometrically predictable patterns, where N containing traits increased with cellular N content, and decreased with increasing C : N ratios. C-based traits increased with cellular C content and C : N ratios under nutrient, particularly N, limitation. The pattern of colony formation was confirmed with field data from Lake Taihu (China), showing an increase in colony size when N was limiting and N : P ratios were low. These findings demonstrate how an explicit coupling of trait-based approaches to ecological stoichiometry can support our mechanistic understanding of responses of cyanobacteria toward shifts in resource availability.

Phosphorus Accumulation in Extracellular Polymeric Substances (EPS) of Colony-Forming Cyanobacteria Challenges Imbalanced Nutrient Reduction Strategies in Eutrophic Lakes

“…Our findings revealed that N limitation enhanced EPS-P accumulation in Microcystis colony cultures, especially the labile P (Table ). Phytoplankton often stored considerable cellular carbohydrates under N limitation or low TN:TP ratios because the excess photosynthetic-fixed C that could not be shunted to growth was presumably accumulated as carbohydrates. ,, After achieving the maximum storage capacity, the excess cellular carbohydrates were excreted as EPS . The promoted EPS production facilitated the EPS-P accumulation (Figure c,d) because it provided a bigger P shelter room in EPS with abundant function groups and phosphate/labile P sorption sites. , Moreover, N limitation promoted Microcystis to exude many protein-like substances (i.e., tyrosine-like substances) by dramatically elevating the capacity of algal cells for N assimilation .…”

“…Phytoplankton often stored considerable cellular carbohydrates under N limitation or low TN:TP ratios because the excess photosynthetic-fixed C that could not be shunted to growth was presumably accumulated as carbohydrates. 25,27,65 After achieving the maximum storage capacity, the excess cellular carbohydrates were excreted as EPS. 27 The promoted EPS production facilitated the EPS-P accumulation (Figure 3c,d) because it provided a bigger P shelter room in EPS with abundant function groups and phosphate/labile P sorption sites.…”

“…22,24 Nitrogen can play an important role in the regulation of EPS production in cyanobacteria. 25−27 Specifically, N limitation can often elevate EPS production, 27 alter EPS structure and composition, 28 and then shape the morphology and colony size of cyanobacterial aggregates. 26 The imbalanced nutrient reduction is thus likely to promote the cyanobacterial capacity for P storage in their EPS and then increase the total cyanobacterial particulate P quota (including both P stored in EPS and cells).…”

“…In world’s large bloom-impacted lakes, such as Lake Taihu (China) and Lake Champlain (Canada/USA), , nitrogen (N) concentration often tended to be scarce with the development of cyanobacterial blooms, presumably a result of the high rate of denitrification . Consequently, cyanobacterial aggregates generally experienced strict N limitation when the blooms reached their peak biomass. , The intensity of N limitation is expected to be stronger because of the imbalanced nutrient reduction efforts/efficiencies, for example, along with the substantial and constant reductions of N concentration and nutrient stoichiometry (i.e., TN:TP ratios) in Lake Taihu during the past decade. , Nitrogen can play an important role in the regulation of EPS production in cyanobacteria. − Specifically, N limitation can often elevate EPS production, alter EPS structure and composition, and then shape the morphology and colony size of cyanobacterial aggregates . The imbalanced nutrient reduction is thus likely to promote the cyanobacterial capacity for P storage in their EPS and then increase the total cyanobacterial particulate P quota (including both P stored in EPS and cells).…”

Dynamic Phycobilin Pigment Variations in Diazotrophic and Non-diazotrophic Cyanobacteria Batch Cultures Under Different Initial Nitrogen Concentrations

“…Microcystis may re-direct C metabolism toward glycogen accumulation in response to N starvation, which causes an increase in C: N ratios ( Forchhammer and Selim, 2020 ). In addition, elevated C: N ratio in Microcystis may be attributed to the formation of C-rich polysaccharide under N-limited conditions ( Duan et al, 2021 ), thereby cells may cluster together to form colonies. Colonial Microcystis blooms are commonly found in field studies, and a series of abiotic and biotic factors may induce colony formation ( Xiao et al, 2018 ), which in turn provides Microcystis spp.…”