Schindler's legacy: from eutrophic lakes to the phosphorus utilization strategies of cyanobacteria

Abstract

David Schindler and his colleagues pioneered studies in the 1970s on the role of phosphorus in stimulating cyanobacterial blooms in North American lakes. Our understanding of the nuances of phosphorus utilization by cyanobacteria has evolved since that time. We review the phosphorus utilization strategies used by cyanobacteria, such as use of organic forms, alternation between passive and active uptake, and luxury storage. While many aspects of physiological responses to phosphorus of cyanobacteria have been measured, our understanding of the critical processes that drive species diversity, adaptation and competition remains limited. We identify persistent critical knowledge gaps, particularly on the adaptation of cyanobacteria to low nutrient concentrations. We propose that traditional discipline-specific studies be adapted and expanded to encompass innovative new methodologies and take advantage of interdisciplinary opportunities among physiologists, molecular biologists, and modellers, to advance our understanding and prediction of toxic cyanobacteria, and ultimately to mitigate the occurrence of blooms.

Keywords: Cyanobacterial blooms; Michaelis-Menten; Monod; eutrophication; nutrient limitation; phytoplankton.

Figure 1.

Conceptual diagram illustrating molecular mechanisms in phosphorus (P) uptake, metabolism and storage by a cyanobacterial cell. The bacteria on cyanobacterial cell walls suggests that that they are also involved in utilizing organic P metabolism. Black dashed arrows indicate the transport pathways of P and solid arrows indicate metabolism of P. Ovals—P pools, squares—phosphate-processing enzymes or regulatory proteins, rounded green squares—transporter protein complexes. DOP = dissolved organic P, Pi = orthophosphate, POP = particulate organic P, AP = alkaline phosphatase, NT = 5’-nucleotidase, Acid P = acid phosphatases, ADP = adenosine di-phosphate, ATP = adenosine triphosphate, polyP = polyphosphate, PPX = exophosphatase.

Figure 2.

Summary of phosphorus (P) fractions measured in water and sediment samples, including ICP-MS (inductively coupled plasma mass spectrometry) for TP, sequential extraction of P components followed by colorimetry, NMR (nuclear magnetic resonance of individual P components), and digestion followed by colorimetry for TP. The analytical techniques are considered surrogates or proxies for P availability to phytoplankton. Red dashed arrows indicate a varying condition where a fraction of PIP, POP and DOP is available depending on the P forms and phytoplankton species. Other abbreviations are: Ca-P—calcium-bound P (apatite P etc.), Fe-P—iron-bound P, Mn-P—manganese-bound P, Al-P—aluminium-bound P, Fe-P—iron-bound P, TPP—total particulate P, TDP—total dissolved P, POP—particulate organic P, PIP—particulate inorganic P, DIP—dissolved inorganic P, DOP—dissolved organic P. Colloidal P includes a small fraction of dissolved inorganic P and some particulate organic P. FRP = filterable reactive P, and when evaluating these filterable P, MRP (molybdate reactive P) = SRP (soluble reactive P) = FRP. For total reactive P, MRP = SRP + a fraction of particulate P. The P fractions from the sequential extraction are examples using different extraction methods (Chang and Jackson , Peryer-Fursdon et al. 2015).

Figure 3.

Conceptual diagram illustrating dynamics of P affecting cyanobacterial metabolism and growth in a lake. Background colour (white—low, blue—high) in the water column represents the gradient of ambient P concentration (Pi, DOP) which increases from the surface to the bottom. Black arrows indicate the transport pathways and metabolism of P. DOP = dissolved organic P, Pi = orthophosphate, POP = particulate organic P. The green symbols indicate phytoplankton, and the yellow symbol indicates bacteria that attach phytoplankton cells. Note that this is a simplification and does not include interactions with particulate inorganic P that can adsorb or desorb P according to inorganic sediment properties (sorption isotherms), Pi concentrations and environmental variables (e.g. temperature, dissolved oxygen).

Figure 4.

Comparison of cellular uptake of orthophosphate ions (Pi) simulated at an instantaneous value, i.e. for a given Q and Pi at that instance in time, using four equations: (a) comparison of the integrated Michaelis-Menten kinetics and Droop quota model in Equation 3.4 (surface plot) and the conventional Michaelis-Menten kinetics in Equation 3.2 (dashed lines with a given intracellular P quota values denoted); (b) comparison of Equation 3.4 given at the minimum intracellular P quota (black dashed line) with the linear flow-force model in Equation 3.5 (blue dashed line), and the non-linear flow-force in Equation 3.6 (red dashed line); and (c) comparison of Equation 3.4 given at the maximum Pi ( = 0.2 mg L-1) (black dashed line) and the Baird's Chemical kinetics (CR) model in Equation 3.7 (red dashed line). The data were adopted from Pi uptake kinetics of a Microcystis aeruginosa strain characterized using Michaelis-Menten kinetics (Suominen et al. 2017) with = 1.88 fmol P cell-1, = 0.285 fmol P cell-1, = 0.093 mg L-1, = 1.853 fmol P cell-1 d-1, extracellular Pi concentration from 0 to 2 mg L-1, with uptake rates and corresponding extracellular Pi concentrations used to parameterise the linear flow-force model ( = 0.79 fmol P cell-1 d-1, = 0.61 µg L-1), and non-linear flow-force model ( = 0.26 fmol P cell-1 d-1, = 0.197 mg L-1, L = 0.008 fmol P cell-1 d-1, m = 3). The Baird-Emsley model (Baird and Emsley , Baird et al. 2001), referred to as a chemical kinetics (CR) model, was fitted using the same and as in the Michaelis-Menten kinetics ( = 1.3148; see Equation 3.7).

Figure 5.

Violin plot of phosphorus terms and concentrations from published culture studies of freshwater and marine cyanobacteria. As there were lots of zero concentrations in P ‘starv*’, ‘deplet*’, ‘limit*’ and ‘deficien*’ treatments, P concentrations were transformed by applying log10(x + 1), where x is the individual P concentration from each study. The shape of the violin shows the probability density of the data. Note that no culture studies from marine cyanobacteria used ‘sufficien*’. For ‘starv*’, laboratory cultures were mostly in media with a given P concentration (i.e. no supply). The terms of ‘deplet*’, ‘limit*’, and ‘deficien*’ were sometimes used interchangeably within a study.