The gut commensal bacterium Enterococcus faecalis LX10 contributes to defending against Nosema bombycis infection in Bombyx mori

Abstract

BACKGROUND: Microsporidia, a group of obligate intracellular fungal-related parasites, have been used as efficient biocontrol agents for agriculture and forestry pests due to their host specificity and transovarial transmission. They mainly infect insect pests through the intestinal tract, but the interactions between microsporidia and the gut microbiota of the host have not been well demonstrated.RESULTS: Based on the microsporidia-Bombyx mori model, we report that the susceptibility of silkworms to exposure to the microsporidium Nosema bombycis was both dose and time dependent. Comparative analyses of the silkworm gut microbiome revealed substantially increased abundance of Enterococcus belonging to Firmicutes after N. bombycis infection. Furthermore, a bacterial strain (LX10) was obtained from the gut of B. mori and identified as Enterococcus faecalis based on 16S rRNA sequence analysis. E. faecalis LX10 reduced the N. bombycis spore germination rate and the infection efficiency in vitro and in vivo, as confirmed by bioassay tests and histopathological analyses. In addition, after simultaneous oral feeding with E. faecalis LX10 and N. bombycis, gene (Akirin, Cecropin A, Mesh, Ssk, DUOX and NOS) expression, hydrogen peroxide and nitric oxide levels, and glutathione S-transferase (GST) activity showed different degrees of recovery and correction compared with those under N. bombycis infection alone. Finally, the enterococcin LX protein was identified from sterile LX10 fermentation liquid based on liquid chromatography-tandem mass spectrometry (LC-MS/MS) analysis.CONCLUSION: Altogether, the results revealed that E. faecalis LX10 with anti-N. bombycis activity might play an important role in protecting silkworms from microsporidia. Removal of these specific commensal bacteria with antibiotics and utilization of transgenic symbiotic systems may effectively improve the biocontrol value of microsporidia.

The Intestinal Immune Defense System in Insects

“…In mosquitoes, ROS, metabolites, small peptides, and proteins secreted by gut bacteria may directly influence the transmission and development of pathogens [ 98 ]. A recent study also confirmed that the Bombyx mori intestinal commensal Enterococcus faecalis LX10 significantly reduced the germination rate and effectiveness of infection by the microsporidium Nosema bombycis [ 99 ]. Meanwhile, intestinal commensal bacteria activate the Imd–Relish immune pathway to balance the regeneration of intestinal epithelial cells caused by pathogenic bacteria [ 100 ].…”

Bacterial biota associated with the invasive insect pest Tuta absoluta (Meyrick)

“…Enterococcus have also been reported to increase larval defense of Bombyx mori to biological control and removal of the Enterococcus symbiont from the larvae would increase the success of biocontrol of this insect larvae 84 . Enterococcus and Lactococcus can protect insect larvae against pathogens, plant toxins and increase host fitness 54 , 85 .…”

Multiomics analysis reveals the molecular basis for increased body weight in silkworms (Bombyx mori) exposed to environmental concentrations of polystyrene micro- and nanoplastics

“…Recent studies have also revealed the importance of the silkworm gut microbiome in various aspects of host physiology, including nutrient metabolism, disease resistance, and immune defense [25] , [54] , [58] , [59] . Exposure to PS-MNPs can change the structure of the microbial community, with smaller particles having a stronger impact.…”

“…The enrichment of genera Acinetobacter and Enterococcus in the exposure groups, positively correlated with body weight, suggests that they might be potential biomarkers for obesity. These taxa have health-promoting potential and an improved capacity for energy harvest and storage, leading to increased caterpillar body weights [54] , [58] , [59] , [62] , [63] . In accordance with our study, these taxa were strongly associated with the gut microbiota of G. mellonella, Tenebrio molitor, and Tribolium castaneum which had consumed PS-MNPs and other kinds of plastics [21] , [22] , [64] .…”