Abstract
Iron (Fe) is an essential nutrient for microalgal metabolism. The low solubility of Fe in oxic aquatic environments can be a growth-limiting factor for phytoplankton. Synthetic chelating agents, such as ethylenediaminetetraacetic acid (EDTA), are used widely to maintain Fe in solution for microalgal cultivation. The non-biodegradable nature of EDTA, combined with sub-optimal bioavailability of Fe-EDTA complexes to microalgae, indicates opportunity to improve microalgal cultivation practices that amplify production efficiency and environmental compatibility. In the present study, the effects of four organic chelating ligands known to form readily bioavailable organic complexes with Fe in natural aquatic environments were investigated in relation to growth and biochemical composition of two marine microalgae grown as live feeds in shellfish hatcheries (Chaetoceros calcitrans and Tisochrysis lutea). Three saccharides, alginic acid (ALG), glucuronic acid (GLU), and dextran (DEX), as well as the siderophore desferrioxamine B (DFB), were compared to EDTA. Organic ligands characterized by weaker binding capacity for cationic metals (i.e., ALG, GLU, DEX) significantly improved microalgal growth and yields in laboratory-scale static batch cultures or bubbled photobioreactors. Maximal microalgal growth enhancement relative to the control (e.g., EDTA) was recorded for GLU, followed by ALG, with 20–35% increase in specific growth rate in the early stages of culture development of C. calcitrans and T. lutea. Substitution of EDTA with GLU resulted in a 27% increase in cellular omega 3-polyunsaturetd fatty acid content of C. calcitrans and doubled final cell yields. Enhanced microalgal culture performance is likely associated with increased intracellular Fe uptake efficiency combined with heterotrophic growth stimulated by the organic ligands. Based upon these results, we propose that replacement of EDTA with one of these organic metal-chelating ligands is an effective and easily implementable strategy to enhance the environmental compatibility of microalgal cultivation practices while also maximizing algal growth and enhancing the nutritional quality of marine microalgal species commonly cultured for live-feed applications in aquaculture.
Highlights
Microalgal biomass and derived products are biological resources relevant to various products in the feed, food, energy, and pharmaceutical sectors (Vanthoor-Koopmans et al 2013; Enzing et al 2014; Koller et al 2014)
In the present study, we examined the efficacy of organic metal-chelating ligands as ethylenediaminetetraacetic acid (EDTA) alternatives in microalgal growth media and assessed performance of two key marine microalgal species (Chaetoceros calcitrans and Tisochrysis lutea) used for the production of live aquaculture feeds (Guedes and Malcata 2012; Brown and Blackburn 2013)
Organic metal-chelating ligands applied at equivalent dosage as EDTA in the growth medium, as well as a fivefold enhancement factor for glucuronic acid (GLU), were shown to have significant effects on the growth performance of C. calcitrans and T. lutea, under both static and bubbled culture conditions (Tables 1, 2, and 3; Figs. 1 and 2)
Summary
Microalgal biomass and derived products are biological resources relevant to various products in the feed, food, energy, and pharmaceutical sectors (Vanthoor-Koopmans et al 2013; Enzing et al 2014; Koller et al 2014). Iron (Fe) nutrition is essential for phytoplankton metabolism This nutrient is required for numerous biological processes (e.g., photosynthesis and respiration, chlorophyll synthesis, and detoxification of reactive oxygen species) (Sunda and Huntsman 1995a; Marchetti and Maldonado 2016) that significantly affect algal productivity and biomass composition (Liu et al 2008). To compensate for low Fe bioavailability (defined here as the degree to which a Fe-substrate can be accessed and utilized by an organism), a plethora of inorganic and organic processes have evolved to enable phytoplankton to meet Fe requirements in oxic aquatic environments where dissolved “free” (unchelated) Fe can be growth-limiting (Morel et al 2008; Shaked and Lis 2012). The processes and factors governing Fe bioavailability are multifaceted, with aspects of Fe speciation and kinetics, phytoplankton physiology, light, temperature, and microbial interactions all intricately intertwined (Bruland et al 1991; Sunda and Huntsman 1995b; Worms et al 2006; Shaked and Lis 2012). Complex feedbacks exist between microorganisms and Fe wherein biologically produced, Fe-chelating molecules (e.g. exopolymeric substances and siderophores) can influence Fe chemistry with consequences for bioavailability (Völker and Wolf-Gladrow 1999; Shaked and Lis 2012; Hassler et al 2015)
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