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Relative contributions of egg-associated and substrate-associated microorganisms to black soldier fly larval performance and microbiota.

ABSTRACT: Larvae of the black soldier fly (BSF) can be used to convert organic waste into insect biomass for animal feed. In this process, they interact with microorganisms originating from the substrate, the insect and the environment. The substrate is the main determinant of the larval gut microbiota composition, but inoculation of the substrate with egg-associated bacteria can improve larval performance. We aimed to quantify the relative importance of substrate-associated and egg-associated microorganisms in BSF larval performance, bacterial abundance and bacterial community composition, when larvae were fed with chicken feed or chicken manure. For this, we inactivated substrate-associated microorganisms by autoclaving, or disinfected BSF eggs. Larval survival, weight and proportion of prepupae were determined on day 15. We collected substrate and larval samples on days 0 and 15 and performed 16S rRNA gene-targeted qPCR and amplicon sequencing. In both chicken feed and chicken manure, egg disinfection did not cause any difference in larval performance or overall microbiota composition. In contrast, in chicken manure, substrate-associated microorganisms increased larval biomass and sterilizing the substrate caused major shifts in microbiota. Thus, substrate-associated microorganisms impact not only larval microbiota but also larval performance, whereas egg-associated microorganisms have a minor role in the densities present.

SUBMITTER: J J Schreven S

PROVIDER: S-EPMC8044291 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Saprophagous fly larvae interact with a rich community of bacteria in decomposing organic matter. Larvae of some species, such as the black soldier fly, can process a wide range of organic residual streams into edible insect biomass and thus produce protein as a sustainable component of livestock feed. The microbiological safety of the insects and substrates remains a point of concern. Substrate-associated bacteria can dominate the larval gut microbiota, but the larvae can also alter the bacterial community in the substrate. However, the relative importance of substrate type and larval density in bacterial community dynamics is unknown. We investigated four larval densities (0 [control], 50, 100, or 200 larvae per container [520 mL; diameter, 75 mm]) and three feed substrates (chicken feed, chicken manure, and camelina substrate [50% chicken feed, 50% camelina oilseed press cake]) and sampled the bacterial communities of the substrates and larvae at three time points over 15 days. Although feed substrate was the strongest driver of microbiota composition over time, larval density significantly altered the relative abundances of several common bacterial genera, including potential pathogens, in each substrate and in larvae fed chicken feed. Bacterial communities of the larvae and substrate differed to a higher degree in chicken manure and camelina than in chicken feed. This supports the substrate-dependent impact of black soldier fly larvae on bacteria both within the larvae and in the substrate. This study indicates that substrate composition and larval density can alter bacterial community composition and might be used to improve insect microbiological safety. IMPORTANCE Black soldier fly larvae can process organic side streams into nutritious insect biomass, yielding a sustainable ingredient of animal feed. In processing such organic residues, the larvae impact the substrate and its microbiota. However, their role relative to the feed substrate in shaping the bacterial community is unknown. This may be important for the waste management industry to determine whether pathogens can be controlled by manipulating the larval density and the timing of harvest. We investigated how the type of feed substrate and the larval density (number of larvae per container) interacted to influence bacterial community composition in the substrates and larvae over time. Substrate type was the strongest driver of bacterial community composition, and the magnitude of the impact of the larvae depended on the substrate type and larval density. Thus, both substrate composition and larval density may be used to improve the microbiological safety of the larvae as animal feed.

Project description:The use of the black soldier fly has been demonstrated to be effective in the treatment of swine manure. Since the outbreaks of ASFV, prevention procedures, including manure disinfection, have changed dramatically. Glutaraldehyde (GA) and potassium peroxymonosulfate (PPMS) have been shown to be effective in the prevention of this pathogen and are thus widely used in the disinfection of swine manures, etc. However, research on the effects of disinfectants in manures on the growth of BSFL and gut microbiota is scarce. The goal of this study was to determine the effects of GA and PPMS on BSFL growth, manure reduction, and gut microbiota. In triplicate, 100 larvae were inoculated in 100 g of each type of manure compound (manure containing 1% GA treatment (GT1), manure containing 0.5% GA treatment (GT2), manure containing 1% PPMS treatment (PT1), manure containing 0.5% PPMS treatment (PT2), and manure without disinfectant (control)). After calculating the larval weight and waste reduction, the larval gut was extracted and used to determine the microbial composition. According to the results, the dry weights of the larvae fed PT1-2 (PT1: 86.7 ± 4.2 mg and PT2: 85.3 ± 1.3 mg) were significantly higher than those of the larvae fed GT1-2 (GT1: 72.5 ± 2.1 mg and GT2: 70 ± 2.8 mg) and the control (64.2 ± 5.8 mg). There was a 2.8-4.03% higher waste reduction in PT1-2 than in the control, and the waste reduction in GT1-2 was 7.17-7.87% lower than that in the control. In a gut microbiota analysis, two new genera (Fluviicola and Fusobacterium) were discovered in PT1-2 when compared to GT1-2 and the control. Furthermore, the disinfectants did not reduce the diversity of the microbial community; rather, Shannon indices revealed that the diversities of GT1-2 (GT1: 1.924 ± 0.015; GT2: 1.944 ± 0.016) and PT1 (1.861 ± 0.016) were higher than those of the control (1.738 ± 0.015). Finally, it was found that both disinfectants in swine manures at concentrations of 1% and 0.5% may be beneficial to the complexity and cooperation of BSFL gut microbiota, according to an analysis of microbial interactions.

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Relative contributions of egg-associated and substrate-associated microorganisms to black soldier fly larval performance and microbiota.

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