The influence of iron, siderophores and refractory DOM on cyanobacterial biomass in oligotrophic lakes

Abstract

Summary Our conceptual understanding of factors that promote cyanobacterial growth is inadequate in the face of rising public concern about cyanobacterial blooms in oligotrophic freshwater lakes. We hypothesised that cyanobacterial density would be highest in lakes with low levels of phosphorus (P), nitrogen (N), total dissolved iron (TDFe) and dissolved organic matter (DOM) with labile properties, where cyanobacteria use siderophores to scavenge Fe and overcome Fe limitation. We tested this hypothesis by measuring cyanobacterial density during peak biomass in 25 oligotrophic lakes representing gradients in total P (TP), nitrate, TDFe and DOM concentrations. Total phytoplankton biomass, using chlorophyll‐a (chl‐a) as a proxy, was a function of TP (r2 = 0.83, P < 0.001). Cyanobacterial density was highest in lakes with low chl‐a, low TP, variable (low and high) nitrate and low TDFe. Regression tree analysis confirmed that TDFe, specifically low concentrations (<3.2 μg L−1), gave rise to the highest cyanobacterial densities in lakes. All lakes had detectable concentrations of hydroxamate and/or catecholate siderophores. In lakes with relatively low TDFe (<3.2 μg L−1), cyanobacterial density was positively correlated with hydroxamate siderophore concentration (r2 = 0.77, P = 0.01). In lakes with higher TDFe (≥3.2 μg L−1), cyanobacterial density was positively correlated with nitrate (r2 = 0.84, P < 0.001) and ammonium (r2 = 0.75, P < 0.001) concentrations. Dissolved organic matter may have an overriding control on cyanobacterial density, with cyanobacterial densities typically highest where DOM concentrations were low (<5 mg L−1) and with a humification index <5. These findings suggest that DOM with labile properties may allow cyanobacteria to gain access to Fe complexed with DOM and thus to overcome Fe limitation, while DOM with refractory properties may bind Fe tightly so that Fe is not readily bioavailable to cyanobacteria. A new conceptual model is presented that emphasises the potential influence of DOM quantity and quality on the functioning of siderophores and the provision of a supply of Fe to cyanobacteria in lakes with low macronutrient supply.

Browning reduces the availability—but not the transfer—of essential fatty acids in temperate lakes

“…hydrologic intensification, Senar, Webster, & Creed, 2018) additional refractory DOM inputs led to shifts in phytoplankton communities; while green algae responded positively to higher DOM quantity, cyanobacteria responded positively to shifts in water colour (i.e. Cyanobacteria have been found to have competitive advantages in lakes with moderate concentrations of refractory DOM (Sorichetti et al, 2014). Cyanobacteria have been found to have competitive advantages in lakes with moderate concentrations of refractory DOM (Sorichetti et al, 2014).…”

“…changes in DOM quantity and quality, and thus light conditions and nutrient availability). Cyanobacteria have accessory pigments that allow them to photosynthesise under lower light conditions (Oliver & Ganf, 2000), some species can scavenge Fe from DOM-Fe complexes (Sorichetti et al, 2014(Sorichetti et al, , 2016, and some species can shift from autotrophy to mixotrophy to consume DOM (Poerschmann, Spijkerman, & Langer, 2004;Wilken et al, 2018) in nutrient-poor and dark lake waters. Cyanobacteria have accessory pigments that allow them to photosynthesise under lower light conditions (Oliver & Ganf, 2000), some species can scavenge Fe from DOM-Fe complexes (Sorichetti et al, 2014(Sorichetti et al, , 2016, and some species can shift from autotrophy to mixotrophy to consume DOM (Poerschmann, Spijkerman, & Langer, 2004;Wilken et al, 2018) in nutrient-poor and dark lake waters.…”

“…For example, cyanobacteria have phycobiliproteins, accessory pigments that allow them to photosynthesise under lower-light conditions (Oliver & Ganf, 2000). siderophores) that scavenge Fe from DOM and transport it into the cell (Sorichetti, Creed, & Trick, 2014;Trick & Kerry, 1992). Aphanizomenon sp.)…”

Iron and iron‐binding ligands as cofactors that limit cyanobacterial biomass across a lake trophic gradient

“…However, few field studies have been conducted in freshwater environments (e.g. Murphy et al ., ; Sorichetti et al ., ,b), and to the best of our knowledge, none compares the role of Fe in regulating cyanobacterial biomass across a lake trophic gradient. This study built upon the limited findings available from oligotrophic freshwater environments to explore the relationship between Fe supply and bioavailability to cyanobacterial biomass and Fe‐binding ligand concentrations in temperate lakes that span a range of trophic states from ultra oligotrophic to hypereutrophic.…”

Effect of Fe and EDTA on Freshwater Cyanobacteria Bloom Formation

“…Recently, a few enclosure experiments showed Fe is a potential limiting nutrient for cyanobacterial growth in eutrophic lakes [25,26]. Although the physiological effects of Fe on cyanobacteria and cyanobacteria's Fe uptake mechanisms have been well studied [27,28], the effect of Fe on cyanobacteria bloom formation is not clear. Clarifying this effect is very important for understanding the cyanobacteria bloom mechanism and developing effective eutrophication management strategies.…”