Evidence for iron‐regulated cyanobacterial predominance in oligotrophic lakes

Sorichetti, Ryan J.; Creed, Irena F.; Trick, Charles G.

doi:10.1111/fwb.12295

Cited by 40 publications

(30 citation statements)

References 33 publications

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“…This strategy locks Fe 3+ into siderophore-bound complexes that are unavailable to other algae that do not have a siderophore-Fe uptake system and may act to limit their population growth. Indeed, Sorichetti, Creed and Trick (2014a) found that siderophores lower 'free' (modelled) Fe 3+ to extremely low concentrations. Siderophores do not appear to be responsible for initiating blooms but could be essential in maintaining them by limiting eukaryotic access to Fe (Murphy, Lean & Nalewajko, 1976).…”

Section: Acquiring Fe With Siderophoresmentioning

confidence: 99%

A novel model for cyanobacteria bloom formation: the critical role of anoxia and ferrous iron

et al. 2014

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SUMMARY1. A novel conceptual model linking anoxia, phosphorus (P), nitrogen (N), iron (Fe) and sulphate to the formation of noxious filamentous and colonial cyanobacteria blooms is presented that reconciles seemingly contradictory ideas about the roles of P, N and Fe in bloom formation. 2. The model has several critical concepts: (i) P regulates biomass and productivity in fresh waters until excessive loading renders a system N-limited or light-limited, but it is the availability of ferrous ions (Fe 2+ ) that regulates the ability of cyanobacteria to compete with its eukaryotic competitors; (ii) Fe 2+ diffusing from anoxic sediments is a major Fe source for cyanobacteria, which acquire it by migrating downwards into Fe 2+-rich anoxic waters from oxygenated waters; and (iii) subsequent cyanobacterial siderophore production provides a supply of Fe 3+ for reduction at cyanobacteria cell membranes that leads to very low Fe 3+ concentrations in the mixing zone.3. When light and temperature are physiologically suitable for cyanobacteria growth, bloom onset is regulated by the onset of internal Fe 2+ loading which in turn is controlled by anoxia, reducible Fe content of surface sediments and sulphate reduction rate.4. This conceptual model provides the basis for improving the success of approaches to eutrophication management because of its far-reaching explanatory power over the wide range of conditions where noxious cyanobacteria blooms have been observed.

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Section: Acquiring Fe With Siderophoresmentioning

confidence: 99%

A novel model for cyanobacteria bloom formation: the critical role of anoxia and ferrous iron

et al. 2014

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“…This may be due to the tendency for Fe to bind to DOM in oxic surface waters, which results in Fe-DOM complexes that render Fe nonbioavailable for cellular use while bound (Fujii et al, 2014). Sorichetti et al (2014a) and I.F. Creed (unpubl.…”

Section: Water Chemistry Total Algal and Cyanobacterial Biomassmentioning

confidence: 99%

“…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.…”

Section: Introductionmentioning

confidence: 99%

“…Extracellular Febinding siderophores have been shown to be important sources of Fe to cyanobacteria (Wilhelm & Trick, 1994;Neilands, 1995), in turn regulating important macronutrient uptake. Field-based investigations have provided evidence for the role of Fe in regulating cyanobacterial biomass in lakes in North America (Molot et al, 2010;Sorichetti, Creed & Trick, 2014a) and the use of Fe-binding siderophores that give cyanobacteria a competitive advantage for Fe acquisition when the supply or bioavailability of Fe in lakes is low (Hassler et al, 2009;Sorichetti, Creed & Trick, 2014b).…”

Section: Introductionmentioning

confidence: 99%

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

2015

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Summary The frequency and intensity of cyanobacterial blooms (cyanoblooms) is increasing globally. While cyanoblooms in eutrophic (nutrient‐rich) freshwater lakes are expected to persist and worsen with climate change projections, many of the ‘new’ cyanobloom reports pertain to oligotrophic (nutrient‐poor) freshwater lakes with no prior history of cyanobloom occurrence. Iron (Fe) is required in nearly all pathways of cyanobacterial macronutrient use, although its precise role in regulating cyanobacterial biomass across a lake trophic gradient is not fully understood. In all lakes sampled representing a gradient in trophic status from oligotrophic to hypereutrophic (2.2–561.2 μg L−1 total phosphorus), the relative cyanobacterial biomass was highest at low predicted Fe bioavailability in eutrophic Alberta lakes (<1.0 × 10−22 mol L−1) and low Fe concentration in oligotrophic Ontario Lakes (<3.2 μg L−1). Fe‐binding organic ligands were measured within this range of low bioavailable Fe. Concentrations of ligands with reactive hydroxamate moieties were positively correlated to cyanobacterial biomass in lakes with low Fe bioavailability and supply, suggesting a possible cellular origin (i.e. siderophores) mediated by low Fe. These findings suggest that Fe serves as a possible cofactor that maintains cyanobacterial biomass across a lake trophic gradient and that cyanobacteria invoke a similar Fe‐scavenging system to overcome Fe limitation in lakes of all trophic states.

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“…Among our set of lakes, cyanobacterial density was highest when TDFe concentration was low. This is consistent with laboratory (Kerry et al ., ) and lake (Sorichetti et al ., ) research showing that cyanobacteria are competitive over eukaryotes at low Fe concentrations. Previous research has attributed this competitive advantage to the ability of cyanobacteria when Fe‐limited to use Fe‐binding ligands, hydroxamate and catecholate siderophores.…”

Section: Discussionmentioning

confidence: 99%

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

2014

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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.

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Evidence for iron‐regulated cyanobacterial predominance in oligotrophic lakes

Cited by 40 publications

References 33 publications

A novel model for cyanobacteria bloom formation: the critical role of anoxia and ferrous iron

A novel model for cyanobacteria bloom formation: the critical role of anoxia and ferrous iron

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

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

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