Elsevier

Algal Research

Volume 70, March 2023, 103017
Algal Research

Composition and apparent digestibility coefficients of essential nutrients and energy of cyanobacterium meal produced from Spirulina (Arthrospira platensis) for freshwater-phase Atlantic salmon (Salmo salar L.) pre-smolts

https://doi.org/10.1016/j.algal.2023.103017Get rights and content

Highlights

  • Spirulina meal was evaluated as a low-trophic alternative protein source for salmon.

  • Spirulina meal was rich in nutrients with low antinutritional compounds and contaminants.

  • Single-ingredient digestibility of essential amino acids (EAAs) in Spirulina meal is high.

  • A diet containing 20 % Spirulina meal showed high EAA and n-3 LC-PUFA digestibility.

  • A high-quality protein for salmon based on digestible indispensable amino acid scores (DIAAS)

Abstract

Composition and apparent digestibility coefficients (ADCs) were determined for whole-cell Spirulina meal produced from Arthrospira platensis (UTEX LB 2340). Spirulina meal contained 60 % crude protein, 20 MJ kg−1 gross energy, 16 % nitrogen-free extract (NFE), 10 % ash, 5 % moisture and 4 % crude lipid. Its protein was comprised of 25 % essential (EAAs) and 25 % non-EAAs. Spirulina meal protein demonstrated high EAA indices (1.0–1.3) relative to egg albumin and premium fishmeal. Spirulina meal was rich (mg 100 g−1) in chlorophyll a (1803) and c (369), β-carotene (141) and zeaxanthin (88) with low concentrations of antinutritional compounds crude fibre (4 %), trypsin inhibition activity (7 TUI mg−1) and phytate (17 mg g−1/ g) and undetectable heavy metal contaminants. A substitution digestion assay using cylindro-circular tanks (100L) equipped with faecal settlement columns was conducted with 164 juvenile (25 g) freshwater Atlantic salmon (Salmo salar L.) at 13 °C fed to apparent satiation with a reference diet (100 % basal mixture) or a test diet (80 % basal mixture and 20 % test ingredient) for 7 weeks. Single-ingredient ADCs for Spirulina meal were dry matter (75 %), ash (61 %), protein (81 %), lipid (73 %), NFE (63 %), energy (77 %), EAAs (average 91 %) and polyunsaturated fatty acids (PUFAs, 96 %). Digestible indispensable AA scores (DIAAS) for Spirulina meal were equal to or higher than 1 (range 1.0–4.6) showing Spirulina meal to be a high-quality protein for Atlantic salmon. Diet ADCs for the 20 % Spirulina meal diet were statistically the same as the reference diet for dry matter (73–74 %), ash (36–41 %), crude lipid (93–94 %), NFE (23–32 %) and energy (82–83 %), while crude protein ADC was slightly reduced from 92 to 90 %. Inclusion of 20 % Spirulina meal had no significant effects on diet ADC for the required EAAs (93–98 %), n-6 PUFA (96 %), n-3 PUFA (100 %) or essential n-3 long-chain PUFAs eicosapentaenoic acid and docosahexaenoic acid (100 %).

Introduction

Aquaculture enhances global food security by providing a more sustainable animal protein than traditional capture fisheries and beef production [1], [2]. Atlantic salmon (Salmo salar L.) farming, compared to other aquatic and terrestrial meat-producing animals, is the most efficient at converting feed to muscle accumulation [3], [4]. Salmon aquaculture is currently a net neutral producer of marine protein and continues to reduce its reliance on traditional marine-sourced fish meal and oil in commercial feeds (generally <20 %) [5]. This more judicious use was accomplished through a shift to commercial aquafeed ingredients derived from terrestrial plant-based crops (e.g., soybeans, corn, canola/rapeseed, wheat) and rendered animal ingredients (e.g., poultry and swine processing by-products) [6], [7], [8]. However, this changing paradigm has brought about challenges related to dietary nutrient imbalances such as essential amino acid (EAA) deficiencies, shifting n-3:n-6 polyunsaturated fatty acid (PUFA) ratios [9], introduction of antinutritional compounds [10], altered pellet quality properties [11], compromised fish immune response and disease resistance [12] and reduced levels of healthy n-3 long-chain (LC)-PUFA (chiefly eicosapentaenoic acid, EPA and docosahexaenoic acid, DHA) in final consumer products [13], [14]. Transition to terrestrial ingredients raises ecological sustainability concerns regarding the diversion of potable water and food crops to aquafeeds [15], [16], [17]. To address these issues and to further enable salmon aquaculture to become a net positive producer of marine protein, there is growing research focus on production of new aquafeed ingredients from low-trophic microorganisms like microalgae and cyanobacteria.

Some microorganisms have the potential to address the worsening food/feed ‘protein gap’ through the sustainable industrial mass production (estimated annual production of up to 44 tons of protein per hectare) of high-quality single-cell protein [18]. Many novel ingredients can be produced in sustainable and regenerative ways by transforming certain industrial side streams as cultivation inputs through a circular bioeconomy framework into nutritious raw ingredients [19], [20], [21], [22]. As such, microalgae and cyanobacteria-based aquafeed ingredients are expected to have lower environmental impacts than terrestrial agricultural production through use of non-potable water, reduced deforestation/desertification, smaller areal footprint, lower greenhouse gas (GHG) emissions and competition with human foods [23], [24], [25]. Protein-rich meals produced from the cyanobacteria broadly grouped as ‘Spirulina’ (produced predominantly from A. maxima, A. platensis and other unidentified strains), are among the most promising candidates for animal and aquaculture feed applications. These products have been used as food and feed for centuries and currently have a significant reported annual commercial production of over 72,000 tons [7], [26], [27], [28], [29], [30]. The high potential of these meals are most typically related to their very rapid growth rates and ease of commercial-scale mass cultivation; their high crude protein contents (generally 50–70 % by weight) and suitable amino acid profiles; their supply of other essential macro- and micronutrients, carotenoids and antioxidants; their lack of cell wall recalcitrance; and their wide regulatory acceptance as safe for consumption by humans, animals and fish [18], [19], [31], [32], [33], [34], [35], [36], [37], [38], [39], [40], [41]. Meals evaluated from a variety of Spirulina strains have shown promising results for several non-salmonid finfish species and a small number of salmonid species. The challenge is that many of these studies lack the required biochemical composition and nutrient digestibility data required for adequate evaluation of them as ingredients for farmed fish [42], [43]. Many studies have used poorly defined and/or unspecified Spirulina meal sources; very few have reported ADCs of their test diets; and even fewer still have measured the ‘single-ingredient’ nutrient and energy ADC values of the Spirulina meals under investigation. This study is just the second to report ADC values for essential nutrients and energy of a protein-rich Spirulina meal fed to Atlantic salmon using the widely-accepted substitution digestion assay [44]. While this study reports ADC values using juvenile Atlantic salmon (<25 g) reared in freshwater, the pioneering study of Burr et al. [45] used large Atlantic salmon (>700 g) reared in seawater. Additionally, the Spirulina meal evaluated in this study was produced from a known strain included at 20 % of the diet, while the strain used in the former study was not identified and used at a 30 % inclusion level. The objectives of this study were to comprehensively characterize the biochemical composition of a Spirulina meal produced in land-based photobioreactors from the cyanobacterium Arthrospira platensis (UTEX LB 2340) and to determine juvenile freshwater phase Atlantic salmon-specific ADC values for its essential macronutrients, energy, amino acids and fatty acids.

Section snippets

Spirulina meal

The freshwater cyanobacterium used (Arthrospira platensis strain UTEX LB 2340) was purchased from the Culture Collection of Algae at the University of Texas at Austin. The strain had been maintained at Pond Technologies Inc. (Markham, ON, Canada) until use. For all cultivation steps, SOT nutrient media was used and freshly-prepared in distilled water to contain NaHCO3 (16,800 mg L−1), K2HPO4 (500 mg L−1), NaNO3 (2500 mg L−1), K2SO4 (1000 mg L−1), NaCl (1000 mg L−1), MgSO4 · 7H2O (97.7 mg L−1),

Composition of the Spirulina meal, reference diet and test diet

Proximate, amino acid and fatty acid composition of the Spirulina meal is presented in Table 2, while that of its elemental concentrations, antinutritional components and carotenoid concentrations are presented in Table 3, Table 4. The EAA profile of Spirulina meal (reported in relation to its total protein), its EAA indices (relative to ideally-balanced egg albumin and premium grade high-quality fishmeal), and its DIAAS values (calculated from measured single-ingredient Spirulina meal EAA ADC

Discussion

Detailed knowledge on the biochemical composition (e.g., proximate nutrients, amino acids, fatty acids, minerals, carotenoids, contaminants, etc.) of an aquafeed ingredient is generally the first requirement in its nutritional quality evaluation and that information is widely available for most conventional commonly-used aquaculture feedstuffs. However, the value of that information on its own is limited for the development of nutritionally-complete, high-quality compound aquafeeds. For

Ethical approval

The feeding trial was carried out in accordance with guidelines on the care and use of fish in research, teaching and testing [52].

CRediT authorship contribution statement

Sean M. Tibbetts: Conceptualization, Funding acquisition, Project administration, Methodology, Investigation, Formal analysis, Resources, Supervision, Data curation, Writing – original draft, Writing – review & editing. Margaret J. MacPherson: Methodology, Resources, Data curation, Writing – review & editing. Kyoung C. Park: Methodology, Resources, Data curation, Writing – review & editing. Ronald J. Melanson: Methodology, Resources, Data curation, Writing – review & editing. Shane J.J.

Declaration of competing interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Acknowledgements

Project supports are greatly appreciated from Roumiana Stefanova (NRC, Halifax, NS), Fang Huang (NRC, Ottawa, ON), Nekoo Hosseini, Peter Howard and Tony Di Pietro (Pond Technologies Inc., Markham, ON), Noppawan Chimsung and André Dumas (Center for Aquaculture Technologies Canada, Souris, PE), Alan Donkin (Northeast Nutrition Inc., Truro, NS), Michael Klapperich (Cargill Inc., Omaha, NE), and Yves Gohier (DSM Nutritional Products Canada Inc., Ayr, ON). This project was funded by the National

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