Nutrients limit production of insects for food and feed: an emphasis on nutritionally essential amino acids

Abstract

The growth of the global human population mandates expansion of the agricultural sector to meet food demands. Paradoxically, food waste is detrimentally impacting our land, air, and water. The insects as food and feed sector can bridge these two concerns by recycling organic wastes to produce ingredients for feeding people, livestock, poultry, aquaculture, and pets. The black soldier fly is a key species mass produced for feed and possibly food. This species is globally distributed, not a pest, and can recycle a broad range of organic residues while producing insect biomass (i.e., larvae) that is approved for use globally as a feed ingredient. Currently, there are facilities that can digest 100 tons of organic waste with the black soldier fly daily. However, predicting output from such processes is challenging for numerous reasons. A key limitation of the system is the proper management of diverse wastes. Due to the nutritional complexities of food waste, predicting conversion rates of waste to insect biomass is challenging. In many instances, the ability of the insect to do so could be hampered due to limited nutrients such as nutritionally essential amino acids (EAAs). Determining the impact of EAAs on the life-history traits of the black soldier fly, or any other insect mass produced for such purposes, is critical for optimizing the industry. Given the global human population has already exceeded 8 billion, demand for food will continue to increase. Ironically, while the demand for such resources is increasing, 40% of the food produced is wasted with it either being left unutilized in the field, disposed of due to aesthetics, considered a by-product of no value, or simply not consumed (Surendra et al., 2020). In all instances, such waste is contributing to the erosion of our planet through greenhouse gas production as well as the contamination of soil, air, and water (Girotto et al., 2015; Makanjuola et al., 2020). Developing more efficient (i.e., circular) mechanisms is critical for suppressing, or possibly reversing these negative effects on our planet while feeding the global human population (Borrello et al., 2017). The black soldier fly, Hermetia illucens, (L.) (Diptera: Stratiomyidae; Figure 1) is an innocuous species globally distributed (Kaya et al., 2021). Larvae of this species (Figure 2) have the unique talent of being able to digest most organic substrates while reducing greenhouse gas (Perednia et al., 2017) and noxious odor emissions (Beskin et al., 2018), pathogenic bacteria (Awasthi et al., 2020), toxins (Bosch et al., 2017), and bioremediate heavy metals (Diener et al., 2015). The resulting larvae can be used as feed for various fish species, as well as livestock, poultry, aquaculture, and even pets (Li and Wu, 2020). Furthermore, the resulting digestate (i.e., frass) can be used as a soil amendment (Lopes et al., 2022). In fact, because of its voracious appetite and resulting benefits, it has been industrialized. Adult black soldier fly, Hermetia illucens (photo courtesy of Chelsea Miranda). Larval and prepupal black soldier fly, Hermetia illucens (photo courtesy of Chelsea Miranda). A challenge for using this system is the variation in the nutrient content of the waste (Table 1) being fed to the larvae as it impacts their growth, survivorship, and quality (e.g., protein content). Because of such impacts, research historically has focused on the effects of variation of carbohydrates and crude protein on the process. However, little attention has been directed to the nutritionally essential amino acids (EAAs) that may serve as major bottlenecks preventing optimal waste digestion and production of the black soldier fly. The carbon skeletons of the EAAs are not formed in animal cells but these nutrients are substrates for the synthesis of other proteinogenic amino acids required by all organisms for survival, growth, development, and reproduction (Wu and Li, 2022). Nutritionally essential amino acid profiles in different manures, vegetables, and fruits that potentially can be digested by black soldier fly larvae to produce insect biomass for use as livestock, poultry, aquaculture, and pet foods Notes: Abbreviations: aValues are % of dry matter. bValues are g/100 g wet weight. cValues are g/100 g wet weight. dUSDA values obtained from USDA Nutritional Database: https://fdc.nal.usda.gov/fdc-app.html#/. eList of fruits and vegetables globally produced in 2020 obtained from https://www.statista.com/statistics/264065/global-production-of-vegetables-by-type/. fList of land animals globally produced in 2020 obtained from https://faunalytics.org/global-animal-slaughter-statistics-charts-2022-update/. gList of globally produced fish obtained from https://www.fao.org/3/cc0461en/cc0461en.pdf. hList of grain globally produced obtained from https://www.statista.com/statistics/263977/world-grain-production-by-type/. Nutritionally essential amino acid profiles in different manures, vegetables, and fruits that potentially can be digested by black soldier fly larvae to produce insect biomass for use as livestock, poultry, aquaculture, and pet foods Notes: Abbreviations: aValues are % of dry matter. bValues are g/100 g wet weight. cValues are g/100 g wet weight. dUSDA values obtained from USDA Nutritional Database: https://fdc.nal.usda.gov/fdc-app.html#/. eList of fruits and vegetables globally produced in 2020 obtained from https://www.statista.com/statistics/264065/global-production-of-vegetables-by-type/. fList of land animals globally produced in 2020 obtained from https://faunalytics.org/global-animal-slaughter-statistics-charts-2022-update/. gList of globally produced fish obtained from https://www.fao.org/3/cc0461en/cc0461en.pdf. hList of grain globally produced obtained from https://www.statista.com/statistics/263977/world-grain-production-by-type/. Although an exhaustive review cannot be provided due to space limitations, this summary aims to draw attention to EAAs and their impact on insect biology with the anticipation it will reveal opportunities for future research. By understanding the role of each EAA in black soldier fly production, diets based on food (Figure 3) or other organic wastes for this fly can be tailored to avoid EAA deficiencies and allow optimal conversion of wastes to insect biomass thus enhancing the ability of this industry to protect our planet. Food waste commonly placed in landfills (photo courtesy of Chelsea Miranda). Arginine (Arg) is a member of the glutamine family of amino acids and is a precursor for creatine-an essential component in the energy metabolism of muscles, nerves, and testis of mammals (Tapiero et al., 2002). Arginine is also the precursor of nitric oxide, a signaling molecule that regulates nutrient metabolism in animals (Wu et al., 2021). Arginine is responsible for the detoxification of ammonia, which can be a toxic substance for the central nervous system (Wu et al., 2009). Arginase, an enzyme of the urea cycle, has been reported in several insect species and can be found in the fat body where it functions as a catabolic enzyme for the conversion of arginine into proline (Reddy and Campbell, 1969). This may be especially important in the development of flying insects, as proline plays a crucial role in insect flight-muscle metabolism (Reddy and Campbell, 1969). In Drosophila melanogaster (Meigen; Diptera: Drosophilidae) both proline and arginine showed the greatest potential for improving larval freeze tolerance compared to other amino acids (Koštál et al., 2016), possibly due to the generation of polyamines (putrescine, spermidine, and spermine) that are essential for DNA and protein syntheses (Wu, 2022). Furthermore, high levels of arginine and proline from an artificial diet may alleviate the toxic effects of excessive amounts of ornithine, glycine, or cysteine (Koštál et al., 2016). Histidine (His) is a basic amino acid (Khan et al., 2017) that is critical for insect development and reproduction (Chang, 2004) and is one of the most abundant amino acids in the hemolymph of silkworms, Bombyx mori (L.) (Lepidoptera: Bombycidae; Wyatt et al., 1956). Histamine, which is a biogenic amine synthesized from l-histidine, functions as a neurotransmitter involved in arthropod vision and mechanoreception (Aryal and Lee, 2021). The histaminergic system in Drosophila is involved in regulating physiological responses when exposed to cold temperatures (Aryal and Lee, 2021). Isoleucine (Ile) is a nonpolar, uncharged, branched-chain, aliphatic amino acid (Kisumi et al., 1977). As with all EAAs, isoleucine impacts arthropod growth in general (Nadarajan and Jayaraj, 1975). It can also play a critical role in insect reproduction (Chang, 2004) and chemical ecology (Allison et al., 2004). In the case of reproduction, isoleucine is needed for proper egg formation (Zhou and Miesfeld, 2009). With communication, isoleucine is used to form pheromones that allow insects to locate mates (Zhang et al., 1997). Leucine (Leu) is one of three essential branched-chain amino acids (Wu, 2022). As with other EAAs, deficiencies in leucine impact reproduction through ovarian development restriction (Bodnaryk and Morrison, 1968) as well as insect development and pupation success (Chang, 2004). Limitations in leucine can result in reduced final adult weight (e.g., 50% reduction) as was observed with the confused flour beetle, Tribolium confusum, Duval (Coleoptera: Tenebrionidae; Fraenkel and Printy, 1954). In animal cells, leucine is a potent activator of the mechanistic target of rapamycin cell signaling to stimulate protein synthesis and inhibit proteolysis (Wu, 2022). Lysine (Lys) is a basic amino acid with a linear structure (Khan et al., 2017). Lysine shares the same transmembrane transporter with arginine, histidine, and ornithine to enter cells. Thus, the proper ratio of these four amino acids is crucial for proper nutrition in animals, including insects. Lysine is essential for insect development and reproduction (Chang, 2004). Additional lysine (above 0.3% dietary content) did not improve the growth, development, or nutritional value of larval black soldier flies, but an excess of dietary lysine can be detrimental (reduced larval size, survival, and prepupal rates) due to imbalances among the basic amino acids (Koethe et al., 2022; Wu, 2022). Maximum growth of mealworm, Tenebrio molitor L. (Coleoptera: Tenebrionidae) larvae occurred when the diet included the same concentration of lysine found in reference larval tissue (John et al., 1979). Methionine (Met) is a sulfur-containing amino acid and a precursor of cysteine (Mueller, 1923). It is the major donor of the amino-propyl group and the methyl group for the synthesis of polyamines (spermidine plus spermine) and creatine, respectively, as well as for the methylation of proteins and DNA in animals (Wu, 2022). Compared to other hydrophobic amino acids, the side chain of methionine is not branched, lending to extra flexibility (Aledo, 2019), which increases its binding affinity, antigenicity, and biological and enzymatic activity (Huang and Nau, 2003). Interestingly, methionine is an effective pest management tool against insects with alkaline guts, such as Aedes albopictus (Skuse), Anopheles quadrimaculatus (Say), and Culex tarsalis (Coquillett) mosquitos (Diptera: Culicidae) (Weeks et al., 2019). In other insects, the concentration, and possibly balance with other amino acids, can impact development. For example, in crickets, Acheta domesticus (L.) (Orthoptera: Gryllidae), the inclusion of 1.8% of methionine, inhibited growth compared to the control diet; though, when fed at a lower level (0.45%) or in conjunction with arginine or tryptophan no difference was observed (Neville et al., 1961). The dietary content of methionine can also influence the rate of ingestion in aphids, Myzus persicae (Sulzer; Hemiptera: Aphididae; Mittler, 1967) and a lack of methionine in the diet, or other EAAs for 4 weeks impacted weight gain but not survivorship of yellow mealworm T. molitor larvae (Davis, 1975). For reproductive purposes, methionine-rich storage proteins are more abundant in female pupae (compared to males) and mediate egg formation and pharate adult development in luna moths, Actias luna (L.) (Lepidoptera: Saturniidae) (Pan and Telfer, 1996). Phenylalanine (Phe) is an aromatic amino acid (Hufton et al., 1995). Phenylalanine is a precursor for the biosynthesis of tyrosine, dopamine, noradrenaline, and adrenaline (Lou, 1994). Phenylalanine is needed for immature insect cuticle production (Behmer and Joern, 1993). A lack of or reduction of aromatic amino acids in the diet of developing grasshoppers, Phoetaliotes nebrascensis (Thomas) (Orthoptera: Acrididae), may contribute to a reduction in body size as well as a prolonged developmental time (Behmer and Joern, 1993). As phenylalanine contributes to the sclerotization of the cuticle of immature insects, insects that produce larger or thicker cuticles will require more phenylalanine in their diets during development (Behmer and Joern, 1993). Tyrosine, either ingested directly or synthesized from phenylalanine, is considered to be a rate-determining factor in the melanization reaction responsible for chorion hardening in Aedes aegypti (L.), (Diptera: Culicidae) (Fuchs et al., 2014). Tyrosine metabolites are also important for wound healing, and cuticle tanning, have also been shown to be an essential component of the cell-mediated immune response in insects (Christensen et al., 2005). Threonine (Thr) is an amino acid with a hydroxyl group (Azevedo et al., 2006). Structurally, the side chain of threonine is similar to the side chain of serine, an amino acid that can be synthesized de novo by animal cells (Wu, 2022). Both side chains are exploited by serine/threonine kinases, which are enzymes that transfer phosphates to the oxygen atom of the side chains. One of the most widely studied serine/threonine kinases is protein kinase B (Akt). This enzyme is important as it regulates development and reproduction. For example, in the cigarette beetle, Lasioderma serricorne (Fabricus; Coleoptera: Ptinidae) when an Akt gene was silenced, the insulin signaling pathway was disrupted, which negatively impacted ovarian development, fecundity, carbohydrate metabolism, and juvenile hormone production (Xu et al., 2021). In mosquitoes, A. aegypti, Akt regulates hormone production in females (Riehle and Brown, 2003). Furthermore, in legume pod borers, Maruca vitrata (Fabricus) (Lepidoptera: Crambidae) Akt mediates larval growth under different abiotic (i.e., temperature and diet quality) and biotic (i.e., genetic backgrounds) conditions (Al Baki et al., 2018). Serine and threonine residues are also used by other kinases (Peterson and Schreiber, 1999), which can impact feeding behavior (Ott et al., 2012), egg development (Lu et al., 2016), and immune response (Chiou et al., 1998). Furthermore, threonine is a source of acetyl coenzyme A (Tang et al., 2021), a key participant in many metabolic pathways including protein, carbohydrate, and lipid synthesis. Tryptophan (Trp) is an aromatic amino acid along with phenylalanine and tyrosine (Hufton et al., 1995). Tryptophan is the only amino acid with a bicyclic structure (Lenz et al., 2021). The indole ring on tryptophan provides high hydrophobic features to the molecule, and when tryptophan is metabolized, it can produce biologically active indole compounds (Palego et al., 2016). Tryptophan is essential for growth and is a precursor to several important bioactive compounds including nicotinamide (vitamin B3), serotonin, melatonin, tryptamine, kynurenine, and more (Friedman, 2018). Tryptophan is needed for insect yolk development along with oogenesis (Thomas et al., 1995) as well as pigmentation of insect compound eyes and serosa of the eggs via the kynurenine and 3-hydroxykynurenine (3-HK) pathways (Kikkawa et al., 1955). Adult flesh flies, Neobellieria bullata (Parker) (Diptera: Sarcophagidae), after injection of tryptophan metabolites, suffered from motoric dysfunction ranging in reduction of locomotion to complete paralysis (Cerstiaens et al., 2003). The reproduction of the sweet potato whitefly, Bemisia tabaci (Gennadius) (Hemiptera: Alerodidae), decreased up to 97% after feeding on transgenic plants with upregulated tryptophan decarboxylase (TDC) genes due to the accumulation of tryptamine (Thomas et al., 1995). Valine (Val) is a branched-chain amino acid (BCAA) along with leucine and isoleucine (Skeie et al., 1990). BCAAs are required for the synthesis of proteins and are precursors for the synthesis of alanine, glutamate, and glutamine (Harper et al., 1984; Wu, 2022). BCAAs within invertebrates are transported into the brain by the same carrier that transports the aromatic amino acids, where competition to transport may influence the rate of synthesis of monoamine neurotransmitters, possibly influencing behavior (Skeie et al., 1990). Valine and isoleucine both can contribute a 3-carbon unit to the ethyl-branched portion of JH II (juvenile hormone) (Brindle et al., 1987), which is a very important hormone in insects. JH within insects ensures proper timing of metamorphosis as well as governing aspects of development and reproduction (Jindra et al., 2015), and valine is essential for rapid insect growth (Nadarajan and Jayaraj, 1975). Apisimin, a peptide found in royal jelly from the honey bee, Apis mellifera L. (Hymenoptera: Apidae) is rich in serine and valine and used during larval development (Bíliková et al., 2002). Apisimin has also been found in the heads of both nurse and forager honey bees, concluding it is synthesized during the whole life span of honey bees (Klaudiny et al., 1994). Although a tremendous amount of information is available on the impact of EAAs on specific insect species, including insect development, reproduction, and survival, very little is available to date for insects that are mass produced for food or feed, such as the black soldier fly. Similarly, numerous raw materials (i.e., manure, see Table 1) that can be used for the mass production of insects have not been described in detail, creating black boxes of uncertainty with regard to their value to the industry. Determining minimal thresholds to allow for optimal production of these species is critical for enhancing the efficiency and positive impacts (e.g., quick recycling of waste to minimize greenhouse gas or pathogenic bacteria) associated with such systems. Given the industrialized production of any insect is reliant on fertile egg production (i.e., the cornerstone for the mass production of fertile eggs that results in larvae that digest waste for protein production), optimizing EAAs and other biosynthesizable proteinogenic amino acids in the diet is critical (Wu, 2018). 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