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. 2022 Oct;15(10):2631-2644.
doi: 10.1111/1751-7915.14113. Epub 2022 Jul 26.

Hermetia illucens L. larvae-associated intestinal microbes reduce the transmission risk of zoonotic pathogens in pig manure

Yuanpu Zhang  1   2 , Xiaopeng Xiao  1   2 , Osama Elhag  1   2   3 , Minmin Cai  1   2 , Longyu Zheng  1   2 , Feng Huang  1   2 , Heather R Jordan  4 , Jeffery K Tomberlin  5 , Sing-Hoi Sze  6 , Ziniu Yu  1   2 , Jibin Zhang  1   2
Affiliations

Hermetia illucens L. larvae-associated intestinal microbes reduce the transmission risk of zoonotic pathogens in pig manure

Yuanpu Zhang et al. Microb Biotechnol. 2022 Oct.

Abstract

Black soldier fly (BSF) larvae are considered a promising biological reactor to convert organic waste and reduce the impact of zoonotic pathogens on the environment. We analysed the effects of BSF larvae on Staphylococcus aureus and Salmonella spp. populations in pig manure (PM), which showed that BSF larvae can significantly reduce the counts of the associated S. aureus and Salmonella spp. Then, using a sterile BSF larval system, we validated the function of BSF larval intestinal microbiota in vivo to suppress pathogens, and lastly, we isolated eight bacterial strains from the BSF larval gut that inhibit S. aureus. Results indicated that functional microbes are essential for BSF larvae to antagonise S. aureus. Moreover, the analysis results of the relationship between the intestinal microbiota and S. aureus and Salmonella spp. showed that Myroides, Tissierella, Oblitimonas, Paenalcalignes, Terrisporobacter, Clostridium, Fastidiosipila, Pseudomonas, Ignatzschineria, Savagea, Moheibacter and Sphingobacterium were negatively correlated with S. aureus and Salmonella. Overall, these results suggested that the potential ability of BSF larvae to inhibit S. aureus and Salmonella spp. present in PM is accomplished primarily by gut-associated microorganisms.

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Conflict of interest statement

The authors declare they have no conflict of interests.

Figures

FIGURE 1
FIGURE 1
Effects of BSF larvae on pathogen populations in PM. Impacts of BSF larvae on S. aureus (A) and Salmonella spp. (B) in PM. PM as a control. Each point represents the mean of three independent trials (n = 3). Results :Evaluation of BSF larvae efficiency in reducing natural pathogen populations in PM.
FIGURE 2
FIGURE 2
Effects of intestinal microbes on pathogen populations in PM. Effect of BSF larvae on S. aureus (A) and Salmonella spp. (B) by inoculating with conventional BSF larvae (BSF‐N), sterile BSF larvae (BSF‐S) and sterile BSF larvae with intestinal extracting solution (BSF‐I) in PM. PM as a control (CK). Each point represents the mean of three independent trials (n = 3). Results :Intestinal microbes enhance the ability of BSF larvae to antagonise pathogens.
FIGURE 3
FIGURE 3
Inhibition of S. aureus by the intestinal microorganisms of BSF larvae in vitro. Note: ①②: B. velezensis D2406 fermentation; ③④: B. velezensis D2406 fermentation supernatant; ⑥⑦: B. subtilis BSF‐CL fermentation; ⑧⑨: B. subtilis BSF‐CL fermentation supernatant; ⑤⑩: LB medium. Results :Intestinal microorganisms of BSF larvae antagonise pathogens in vitro.
FIGURE 4
FIGURE 4
Effect of intestinal bacterial inhibition of S. aureus in vivo. CK: non‐intestinal bacteria group. Statistical analyses were performed using unpaired t‐test (*p < 0.05, **p < 0.01, ***p < 0.001) compared with CK. Results:Intestinal microorganisms of BSF larvae antagonise pathogens in vivo.
FIGURE 5
FIGURE 5
BSF larval intestinal bacterial communities in manure conversion systems. Abundance profiles of BSF larva intestinal bacteria at phylum (A) and genus levels (B). (C) Shannon indices for each group sample (n = 3), different letters indicate significant differences (p < 0.05); (D) tb‐RDA of pathogens (S. aureus and Salmonella spp.) and intestinal genus communities in BSF larva converting PM system. Note: IM00: intestinal microbes of initial BSF larvae. IM02, IM04, IM06 and IM08: intestinal microbes of BSF larvae at the second, fourth, sixth and eighth day after the conversion of PM respectively.
FIGURE 6
FIGURE 6
Abundance profiles of PM bacteria at phylum (A, B) and genus levels (C, D). Note: IPM00: fresh PM; PMIL02, PMIL04, PMIL06 and PMIL08: samples of PM converted by BSF larvae at 2, 4, 6 and 8 days respectively. PM02, PM04, PM06 and PM08: samples of PM not inoculated with BSF larvae at 2, 4, 6 and 8 days. Results:Analysis of PM microbial community.
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