AbstractEnteric bacteria can play an important role in the developmental performance of their insect hosts. The present study revealed that two dominant enteric bacteria, Enterococcus mundtii and Enterococcus casseliflavus, are present in the gut of Spodoptera frugiperda larvae on different host plants (maize and rice). However, the role of the two dominant bacteria in S. frugiperda remains poorly understood. To clarify the functions of E. mundtii and E. casseliflavus, the effects on the growth and development of S. frugiperda were studied by separately adding them to an artificial diet with different proportions of yeast. To elucidate the physiological metabolism underlying the differential effects of these two enteric bacteria on the developmental performance of S. frugiperda, transcriptome sequencing was conducted. The results showed that under a rich diet (with 1.85% yeast extract), E. casseliflavus significantly inhibited larval growth and prolonged the pupal stage, under a poor diet (without yeast extract), larval survival rates decreased, but larval body weight increased, and pupal weight significantly increased. However, E. mundtii had no significant effect on S. frugiperda fed a nutritionally rich diet or poor diet. These results indicate that E. casseliflavus exerts a nutrient-dependent effect on life history traits, while E. munditi has little significant impact on the developmental performance of S. frugiperda. Transcriptome sequencing analysis of differential gene expression revealed significant suppression of genes related to physiological metabolism and carbohydrate transport in E. casseliflavus. For instance, the downregulation of UDP-glycosyltransferase (UGT) and amino acid genes is closely associated with the growth and development of Spodoptera frugiperda.These findings provide deeper insights into its impact on the growth and development of S. frugiperda.
IntroductionEnteric bacteria have an inseparable relationship with their host insects, associated with nutritional metabolism1, defense and protection2, immune regulation3, insecticide resistance4, and growth and development of host insects5. The main functions of enteric bacteria on insect growth and development can be divided into promotion, inhibition, and no effect. For example, previous studies have shown that enteric bacteria can increase the weight of young adult bees6. The enteric symbiotic bacterium Klebsiella michiganensis BD177 can increase the survival time of antibiotic-treated the oriental fruit fly Bactrocera dorsalisto the level of normal fruit flies under low-temperature stress of 10 °C7. Meanwhile, some enteric bacteria have inhibitory effects on host insects, such as lactate produced by the microbiota shortens the lifespan of the fruit fly Drosophila8.Fall armyworm, Spodoptera frugiperda, is a new invasive insect in China, which has a wide range of host plants and poses a long-term threat to food production security. Although S. frugiperda invading China preferentially feeds on and oviposits on maize, a considerable portion of S. frugiperdaindividuals can complete their life cycle on young rice plants9,10,11. Previous studies have revealed significant differences in the gut microbiota composition of S. frugiperdathat feed on different host plants12,13.The potential role of enteric bacteria in the adaptation of S. frugiperda to switch its host from maize to rice warrants further investigation.Until now, a large number of enteric bacteria have been identified in S. frugiperda, including Firmicutes and Proteobacteria as dominant phyla in their gut14,15 and Enterococcusas the dominant genus among their gut microbiota14,15,16. Recent research found some enteric bacteria in S. frugiperdacan regulate plant defense responses2, or affect the growth and development of S. frugiperda13, or could degrade insecticides16,17. Additionally, previous studies have shown that the inoculation of enteric bacteria under different nutritional conditions has varying effects on insect growth and development18.However, the relationship between the dominant enteric bacteria and S. frugiperda remains poorly understood. We speculate that the dominant enteric bacteria may influence the growth performance of S. frugiperda, and that this influence is closely related to nutrient supply.The aim of this study was to clarify the effects of the dominant enteric bacteria on the growth and development of S. frugiperda and mechanism underlying it. Firstly, we identified the dominant enteric bacteria using 16 S rDNA full-length high-throughput sequencing technology.Then, the effects on the growth and development of S. frugiperda were studied by separately adding them to an artificial diet with different proportions of yeast to clarify the functions of the dominant enteric bacteria. Finally, the transcriptome sequencing was conducted to elucidate the physiological metabolism underlying the differential effects of these two enteric bacteria on the developmental performance of S. frugiperda. This study will provide valuable insights into the molecular mechanisms underlying the interaction between enteric bacteria and the growth and development of S. frugiperda.Materials and methodsInsectsSpodopterta frugiperda larvae were gathered from a cornfield in Qingdao (120.356436°E, 36.300479°N) and nurtured either on corn (cultivar: ZD958) or rice (japonica rice variety: SD18; indica rice variety: YZX), under temperatures of 25 ± 2 °C, relative humidity 60 ± 5%, and a light-dark cycle of 16:8 h. Adults were confined in polyamide cages (45 cm × 35 cm × 50 cm) with 120 mesh screening and provided a 10% honey solution. Under these conditions, the adults had the opportunity to engage in mating and laying eggs. Newly hatched larvae derived their nutrients from freshly grown corn or rice plants for multiple generations.Collection of spodoptera frugiperda larval intestinesThe 4th instar larvae were chosen from S. frugiperda populations reared on corn, japonica rice, and indica rice. Subsequently, they were placed in a sterile plastic Petri dish that had a small hole in the lid. After 24 h of starvation, larvae were grouped and complete intestines were dissected on a sterile workbench and stored in 1.5 ml sterile centrifuge tubes. Fifteen larvae were pooled as one sample, and each sample had 4 replicates. All samples were stored in a − 80 °C freezer.16 S rDNA sequencing analysisThe larval gut samples collected were subjected to DNA sequencing analysis using the PacBio platform provided by Beijing BioMarker Biotechnology Co., Ltd. The bacterial community within the gut of S. frugiperda larvae was analyzed using full-length 16 S rDNA gene sequencing. The PacBio sequencing platform employs single molecule real-time sequencing (SMRT Cell) technology to sequence the marker gene. Subsequently, the Circular Consensus Sequencing (CCS) data undergoes filtering, clustering, or denoising processes. Finally, species identification and quantitative analysis of their abundance are conducted.The initial dataset underwent correction, identification, and filtration processes. Sequences failing to meet length criteria were eliminated, yielding valid sequences (CCS). USEARCH was employed to categorize effective sequences and delineate OTUs (operational taxonomic units) at 97% similarity. OTU species annotation was performed using QIIME2. Species classification utilized consensus blast, based on the Silva database, to determine the most consistent result among multiple optimal alignment outcomes. This process required a minimum sequence similarity of 90%, coverage of 90%, and consistency of 51%. For sequences lacking accurate database matches, a naive Bayesian classifier was first trained to enable accurate feature distinction among classification groups. Subsequently, the classify-sklarn program was used in conjunction with the aforementioned alignment method for annotation. The number of sequences annotated at each classification level for individual samples was documented to ascertain bacterial community composition in S. frugiperda populations. The relative abundance of operational classification units was obtained by normalizing and analyzing the total sequence count in clustering results and the sequence number in each operational classification unit. Community composition at each level was recorded after excluding low-proportion results (< 0.005%).Feed configurationBefore use, the coarse wheat embryo and distilled water underwent sterilization in an autoclaved steam cooker for 30 min. The components were then combined in a blender following the artificial feed formula for S. frugiperda. The process began by mixing 1000 ml of distilled water and 24 g of agar powder in a clean blender, followed by heating to a boil. Subsequently, 1.4 g of choline chloride, 0.28 g of myo-inositol, and 6 ml of corn oil were added to the mixture and boiled. Next, 24 g of yeast powder, 160 g of coarse wheat germ, and 20 g of fine wheat germ were incorporated one at a time and blended thoroughly. A combination of 48 g of corn leaf flour, 9.6 g of casein, and 2.4 pieces of vitamin B complex was introduced once the blender’s temperature decreased to 70 °C. Lastly, 0.4 ml of insect attractants were added at 70 °C and mixed well. The final mixture was transferred to a sterilized glass Petri dish, sealed, and refrigerated at 4 °C. The feed mixture did not contain any antibiotics. A nutrient-deficient diet was prepared by omitting yeast from the recipe.Isolation, identification, and culture of the enteric bacteriaFourth instar larvae were chosen and deprived of food for 24 h to facilitate intestinal extraction. The extracted intestines were then finely chopped and combined with sterile PBS phosphate buffer (pH = 7.4) to create an intestinal content suspension. This suspension underwent serial dilution with PBS phosphate buffer, resulting in six concentration gradients: 10−1, 10−2, 10−3, 10−4, 10−5, and 10−6. Using the dilution plate technique, 100 µL of each gradient was spread on LB solid medium, with three replicates per concentration, and incubated at 37 °C in a constant temperature incubator. Individual colonies exhibiting diverse colors, sizes, and shapes were picked and re-streaked on fresh LB agar plates. To ensure pure monoclonal bacterial strains, each colony underwent purification more than five times. The purified strains were grown in an LB liquid medium to obtain fresh bacterial cultures. A portion of this culture was used for bacterial DNA extraction and sequencing for identification of E. mundtii and E. casseliflavus, while the remainder was mixed with 25% glycerol and stored at − 80 °C in an ultra-low temperature freezer for later use.One milliliter of E. mundtii or E. casseliflavus liquid-glycerol mixture was introduced into 10 ml of Luria broth (LB). This mixture was incubated for 10 to 11 h at 37 °C with agitation at 200 rpm. The resulting fresh bacterial solution was centrifuged and the pellet was resuspended in phosphate-buffered saline (pH = 7.4). The resuspended bacteria were diluted and counted using a blood cell counter. Based on the bacterial concentration, phosphate-buffered saline was added to achieve a final concentration of 1.0 × 108cfu/ml. Artificial feed was cut into 1 cm3 cubes. For the treatment group, 100 µl of the bacterial suspension were added to each cube to reach a concentration of 1.0 × 107 cfu/cm3, while the control group received 100 ul of phosphate-buffered saline per cube. The axenic group served as the control group. The artificial feed cubes were then mixed with either the bacterial suspension or phosphate-buffered saline for feeding experiments.Inoculation treatmentTreatment methods for S. frugiperdacan be referred to the artificial diet feeding method13.Newly laid S. frugiperda eggs were rinsed in 3% sodium hypochlorite solution for 4 min, washed twice with sterilized water, dried in sterile water, and incubated in a sterilized glass petri dish. Newly hatched larvae (recorded on the first day) were reared on sterile feed.When the larvae reached the 2nd instar (Day 3), five larvae were placed in one 9-cm Petri dish with one feed cube supplemented with bacterial suspension or phosphate-buffered saline. Insects were divided into a control group (axenic group), E. mundtii group, and E. casseliflavusgroup. Each group was divided into two feeding treatments and fed with artificial feed containing 0% yeast extract (poor diet) and 1.85% yeast extract (rich diet), respectively. There were 6 feeding treatments in total, with 60 test insects in each treatment. Larval survival was recorded 2 days after feeding until the larvae pupated; each larva was individually numbered and reared separately, with body weight recorded every two days from day 10 to day 16. Fresh feed cubes were replaced every day to avoid bacterial contamination. After weighing the pupae, they were transferred to sterile soil and placed in test tubes for emergence. The soil was sterilized in an autoclave at 121 °C for 20 min prior to use19. Upon emergence, a female and a male adult were paired in mating chambers consisting of a 1 L plastic cup cut at the bottom and placed inside another cup and covered with gauze for ventilation, which was then inverted, and the second cup was placed on top of the first cup.The time and number of larval pupation and emergence were recorded.Transcriptome sequencing and analysis for physiological metabolismAfter extracting the larval intestines from the control, E. mundtii, and E. casseliflavus groups fed on artificial diets with 1.85% yeast extract content, they were placed in 1.5 ml centrifuge tubes and rapidly frozen in liquid nitrogen for 20 min, then stored at − 80 °C. Each treatment consisted of four biological replicates. For RNA extraction and transcriptome analysis, samples were sent to Beijing BMK Biotechnology Co., Ltd. for high-throughput sequencing.After filtering the raw data to remove reads containing adapters and low-quality reads, high-quality data (clean data) were obtained. The high-quality data were aligned to the reference genome of the S. frugiperda(GCA_011064685.1.genome.fa) to assess library quality. Subsequently, StringTie was used to assemble the aligned reads and reconstruct the transcriptome for further analysis. FPKM (Fragments Per Kilobase of transcript per Million fragments mapped) was employed for normalization as a metric to measure the expression levels of transcripts or genes. DESeq2 was utilized for differential analysis of unique genes, and edgeR was used for differential expression analysis. To identify differentially expressed genes, we employed selection criteria that included a Fold Change ≥ 1.5 and a P-value < 0.01. Functional annotation of the differentially expressed genes was performed using databases such as GO and KEGG20,21, followed by enrichment analysis for GO (Gene Ontology) functions and KEGG (Kyoto Encyclopedia of Genes and Genomes) pathways. GO analysis can define and describe genes and proteins to elucidate the function of each gene. The GO annotation system consists of three main components: biological processes, cellular components, and molecular function.Statistical analysisThe larval survival rate, insect body weight, pupal weight and developmental time were recorded. Data were analyzed using SPSS software version 21.0, using Tukey’s honest dominance difference test for multiple comparisons, with a dominance threshold set at P = 0.05. Significant differences in the pupation and eclosion were analyzed using a chi-square test, and parameters were graphed using GraphPad Prism version 8.02.ResultsRelative abundances of enteric bacteria in spodoptera frugiperda fed on different hostsWe dissected the intestines of larvae feeding on different hosts and analyzed the composition and differences of enteric microbiota using 16 S rDNA full-length high-throughput sequencing technology. After sequencing the samples and identifying bacteria through barcoding, a total of 220,670 CCS sequences were obtained. Each sample generated at least 8,173 CCS sequences, with an average of 11,034 CCS sequences per sample. We found that the relative abundance of E. mundtii (Family Enterococcacae and Phylum Firmicutes) and E. casseliflavus (Family Enterococcacae and Phylum Firmicutes) were the highest in all 3 feeding treatments. The relative abundance of E. mundtii in corn, japonica rice, and indica rice were 76.89%, 25.69%, and 57.55%, respectively; and 13.51%, 20.28%, and 20.22% for E. casseliflavus (Fig. 1). Both E. mundtii and E. casseliflavus were the dominant enteric bacteria in the gut of larvae in S. frugiperda. The relative abundance of E. mundtii (Table S1) and E. casseliflavus (Table S2) significantly increased when re-inoculated into S. frugiperda.Fig. 1Relative abundance of Enterococcus mundtii and Enterococcus casseliflavus in the gut of Spodoptera frugiperda under different host feeding treatments (A: corn, B: japonica rice, C: indica rice).Full size imageSurvival rates of spodoptera frugiperda larvaeThe survival rate of S. frugiperda larvae decreased after feeding on 1.0 × 107 cfu/cm3 enteric bacteria. When fed diet without yeast extract, survival rates decreased rapidly from day 6 (Fig. 2A). The larval survival rate in the E. casseliflavus treatment was significantly lower than that of E. mundtii treatment and the control (E. mundtii P = 0.001; control P = 0.023), but there was no significant difference in larval survival between E. mundtii treatment and control (P = 0.24).On a diet of 1.85% yeast extract (Fig. 2B), the survival rate of larvae fed on E. casseliflavus was significantly lower than the control (P = 0.032), but not significantly different from the E. mundtii group (P = 0.096); although the survival rate of E. mundtii was lower than that of the control group, there was no significant difference (P = 0.571).Fig. 2Survival of Spodoptera frugiperda larvae that fed on artificial diet with enteric bacteria (A: diet without yeast extract; B: diet with 1.85% yeast extract). Values with the same letter are not significantly different at the P > 0.05 level (Kaplan-Meier survival analysis followed by Log-rank test).Full size imageEffect of single bacterial supplementation on larval body weight and pupal weight of Spodoptera frugiperdaFor the larvae that fed with the poor diet (Fig. 3A), there was no significant difference between the bacteria feeding treatment and the control (E. mundtii: Day10, P = 1; Day 12, P = 0.656; Day 14, P = 0.697; Day 16, P = 1; E. casseliflavus: Day 10, P = 0.753; Day 12, P = 0.124; Day 14, P = 0.139; Day 16, P = 0.244). The pupal weight of E. casseliflavus feeding group was significantly greater than those of the control and E. mundtii feeding group (control: P = 0.03; E. mundtii: P = 0.028).Fig. 3Body weight per larva and pupa of Spodoptera frugiperda that fed with different enteric bacteria on days 10,12,14,16 (A: diet without yeast extract; B:diet with 1.85% yeast extract).Error bars indicate SEM. Number of larvae tested (diet without yeast extract): Day10, 39–53; Day12, 39–50; Day14, 39–50; Day16, 39–47; number of pupae tested, 38–45. Number of larvae tested (diet with 1.85% yeast extract): Day10, 41–52; Day12, 41–52; Day14, 41–52; Day16, 41–52; number of pupae tested, 38–43. For a given number of days, the values with the same letter were not significantly different at the P > 0.05 level (ANOVA, followed by Tukey’s post-hoc test).Full size imageWhen the larvae were fed an artificial diet with 1.85% yeast extract (Fig. 3B), the body weights of both groups of bacteria-fed larvae were lower than those of the control. Insect larvae fed on E. casseliflavus on days 10–16 weighed significantly less than the control (Day 10, P = 0.008; Day 12, P = 0.003; Day 14, P = 0.001; Day 16, P = 0.002). However, there was no significant difference in larval weights when compared to the E. mundtii feeding group with the control, or with the E. casseliflavus feeding group (control: Day 10, P = 0.265; Day 12, P = 0.369; Day 14, P = 0.114, Day 16, P = 0.152; E. casseliflavus: Day 10, P = 0.285; Day 12, P = 0.103, Day 14, P = 0.24; Day 16, P = 0.221). Besides, there was no significant difference in the pupal weight between the two bacteria-fed groups of larvae and the control (E. mundtii: P = 0.711; E. casseliflavus: P = 0.987).Differences in pupation time and developmental duration of Spodoptera frugiperdaWhen fed diet without yeast extract, no significance in pupation time was found between each bacteria feeding treatment and the control (E. mundtii: P = 0.912; E. casseliflavus: P = 0.887, Fig. 4A). When fed diet with 1.85% yeast extract content (Fig. 4B), the E. casseliflavus group significantly extended its pupation time compared with the control group (P = 0.02), but no significance was observed between E. mundtii feeding group and the control (P = 0.172); there was no significance between the two enteric bacteria groups (P = 0.611). Under both nutritional conditions, there was no significant effect on the developmental time (diet without yeast extract: E. mundtii: P = 0.661, E. casseliflavus: P = 0.763, E. mundtii vs. E. casseliflavus: P = 1; diet with 1.85% yeast extract: E. mundtii: P = 1, E. casseliflavus: P = 0.408, E. mundtii vs. E. casseliflavus: P = 0.382, Fig. 4CD).Fig. 4Pupation time (A: diet without yeast extract; B: diet with 1.85% yeast extract) and developmental duration (C: diet without yeast extract; D: diet with 1.85% yeast extract) of Spodoptera frugiperda that fed on diet with enteric bacteria. Error bars indicate SEM. Number of insects tested for pupation time, A: 38–46; B: 42–49; number of insects tested for developmental duration, C:5–12; D:11–15. Values with the same letter are not significantly different at the P > 0.05 level (ANOVA followed by Tukey’s post-hoc test).Full size imageSurvival of spodoptera frugiperda after pupation and eclosionAfter bacterial treatment, there were no significant changes in pupation rate (diet without yeast extract: E. mundtii: x2 = 0.391, 1 df, P = 0.532, E. casseliflavus: x2 = 0.950, 1 df, P = 0.33, E. mundtii vs. E. casseliflavus: x2 = 2.540, 1 df, P = 0.111, diet with 1.85% yeast extract: E. mundtii: x2 = 0.455, 1 df, P = 0.5, E. casseliflavus: x2 = 2.228, 1 df, P = 0.136, E. mundtii vs. E. casseliflavus: x2 = 0.682, 1 df, P = 0.409, Fig. 5AB) and eclosion rate (diet without yeast extract: E. mundtii: x2 = 0.096, 1 df, P = 0.757, E. casseliflavus: x2 = 1.363, 1 df, P = 0.243, E. mundtii vs. E. casseliflavus: x2 = 2.155, 1 df, P = 0.142,diet with 1.85% yeast extract: E. mundtii: x2 = 0.171, 1 df, P = 0.679, E. casseliflavus: x2 = 1.950, 1 df, P = 0.163, E. mundtii vs. E. casseliflavus: x2 = 0.957, 1 df, P = 0.328, Fig. 5CD) under the two nutrient conditions.Functional annotation and enrichment analysis of differentially expressed genes in the gut of spodoptera frugiperda larvaeCompared to the control group, the E. casseliflavus group had a total of 939 DEGs (differentially expressed genes), including 394 upregulated genes and 545 downregulated genes (Fig. 6A). The E. mundtii group, compared to the control group, had a total of 355 DEGs, including 155 upregulated genes and 200 downregulated genes (Fig. 6B). The E. casseliflavus group had a greater number of DEGs than the E. mundtii group, with more downregulated genes than upregulated genes in both cases.Fig. 5Survival of pupation (A: diet without yeast extract; B:diet with 1.85% yeast extract) and eclosion (C: diet without yeast extract; D: diet with 1.85% yeast extract) of Spodoptera frugiperda that fed with different enteric bacteria. Values with the same letter are not significantly different at the P > 0.05 level (chi-squared tests).Full size imageFig. 6Volcano plots of differentially expressed transcripts in the gut of Spodoptera frugiperda: (A control group and Enterococcus casseliflavus group CK-EC; B control group and Enterococcus mundtii group CK-EM). Red dots represent upregulated differentially expressed genes (DEGs), blue dots represent downregulated DEGs, and gray dots represent non-differentially expressed genes.Full size imageA total of 386 genes from the E. casseliflavus group were successfully annotated by COG (cluster of orthologous groups of proteins), and 124 genes from the E. mundtii group were successfully annotated by COG. The majority of genes in the E. casseliflavus group were enriched in carbohydrate transport and metabolism, as well as translation, ribosomal structure, and biogenesis, followed by secondary metabolites biosynthesis, transport, and catabolism (Fig. 7A). In contrast, the majority of genes in the E. mundtii group were enriched in carbohydrate transport and metabolism, followed by posttranslational modification, protein turnover, and chaperones (Fig. 7B).Fig. 7COG annotation classification statistics of differentially expressed genes in the gut of Spodoptera frugiperda (A: control group and Enterococcus casseliflavus group CK-EC; B: control group and Enterococcus mundtii group CK-EM).The bar charts were constructed through the bioinformatics platform (BMKCloud).Full size imageThrough GO functional enrichment analysis of DEGs, a total of 818 DEGs were identified in the E. casseliflavus group (Fig. 8A). The DEGs in the biological process category were primarily enriched in cellular processes, metabolic processes, biological regulation, and localization, with downregulated genes mainly enriched in metabolic processes. In the cellular component category, DEGs were primarily enriched in cellular anatomical entities. In the molecular function category, DEGs were mainly enriched in entries such as binding, catalytic activity, and structural molecular activity, with downregulated genes primarily enriched in binding and catalytic activity. In the E. mundtii group, a total of 282 DEGs were identified, and the enrichment trends of DEGs were similar to those in the E. casseliflavus group, but the number of DEGs was fewer than in the E. casseliflavus group (Fig. 8B).Fig. 8GO annotation classification statistics of differentially expressed genes in the gut of Spodoptera frugiperda: gene ontology annotation at biological process, cellular component, and molecular function levels (A: control group and Enterococcus casseliflavus group CK-EC; B: control group and Enterococcus mundtii group CK-EM).The bar charts were constructed through the bioinformatics platform (BMKCloud).Full size imageDEGs in E. casseliflavus group were enriched in KEGG pathways including ribosome, carbon metabolism, glycolysis/gluconeogenesis, pentose phosphate pathway, biosynthesis of amino acids, insect hormone biosynthesis, starch and sucrose metabolism, protein export, citrate cycle (TCA cycle), and metabolism of galactose, propionate, glutathione, pyruvate, alpha-Linolenic acid, taurine and hypotaurine, beta-Alanine, arginine, proline, and tyrosine, among which protein export was upregulated (Fig. 9A). DEGs affecting the growth and development of S. frugiperda larvae may be associated with processes such as carbohydrate transport and metabolism as well as lipase and amino acid metabolism(Table 1). In the E. mundtii group, differentially expressed genes were enriched in KEGG pathways including lysosome, drug metabolism-other enzymes, starch and sucrose metabolism, Wnt signaling pathway, oxidative phosphorylation, and ascorbate and aldonate metabolism (Fig. 9B).Additionally, the genes listed in Table 1 did not exhibit significant differences in the E. mundtii group.Fig. 9Enrichment of KEGG pathways for differentially expressed genes in the gut of Spodoptera frugiperda (A: control group and Enterococcus casseliflavus group CK-EC; B: control group and Enterococcus mundtii group CK-EM). Each circle and triangle in the figure represents the number of genes enriched in a specific KEGG pathway. The enrichment factor represents the ratio of the number of differentially expressed genes to all genes in the pathway.The bubble charts were constructed through the bioinformatics platform (BMKCloud).Full size imageTable 1 DEGs and FPKM values related to carbohydrate transport and metabolism, lipase, amino acid metabolism in the gut of Spodoptera frugiperda larvae fed on artificial diet inoculated with Enterococcus casseliflavus.The positive and negative value of log2FC indicates upregulation and downregulation, respectively.Full size tableDiscussionThe present study revealed that the two dominant enteric Enterococcus bacteria, E. mundtii and E. casseliflavus, were present in the larvae of S. frugiperda when fed with rice and corn (Fig. 1). These results were consistent with Jeon et al.15 , which also showed Enterococcus genus has the highest abundance in S. frugiperda. In S. frugiperda, Enterococcaceae, particularly Enterococcussp., is prevalent throughout all developmental stages22. E. mundtii and E. casseliflavus have also been identified in many insects. For instance, E. mundtii isolated from Bombyx morican cause flacherie in the silkworm23. E. mundtii isolated from Ephestia kuehniella, when orally inoculated into the model organism Tribolium castaneum, confers resistance to the insect pathogen Bacillus thuringiensisbut results in shortened lifespan and reduced fertility24. E. casseliflavus isolated from the lepidopteran Spodoptera lituradid not exert beneficial effects on its host25. Recent research showed that the Enterococcusgenus has been found in various Lepidoptera insects26,27, and it is also a dominant microbial group in some Lepidoptera insects, such as S. frugiperda16, Spodoptera littoralis28, Bombyx mandarina and Bombyx mori29, indicating that this bacterial genus may assist insects in digesting and absorbing food in the gut26.Despite their preponderance in lepidopteran larval guts, the role of these two dominant enteric bacteria remains poorly understood. Mason et al.30. revealed that some strains of Enterococcus spp. can promote the utilization of poor dietary substrates by S. frugiperda. However, our present research showed that E. casseliflavus has a negative effect on the life history traits of S. frugiperda on nutritionally rich diet but has no effect on nutritionally poor diet (Figs. 2, 3, 4 and 5), which indicates that this enteric bacterium may provide benefits under poor dietary conditions. Our previous study demonstrated that Enterobacter cloacae and Staphylococcus sciuri extracted from the intestines of S. frugiperdalarvae had negative effects on growth and development, but in cases of insufficient nutrition, the inhibitory effect disappears and instead a promoting effect appears13. In other insects, many enteric bacteria have been found to have a promoting effect under poor dietary conditions and an inhibitory effect under rich dietary or normal dietary conditions. For example, Cai31 conducted a study on the enteric microbiota of B. dorsalis and found that the role of microbiota in promoting larval growth and development depends on different nutritional levels. When nutrients are insufficient, the presence of microbiota is beneficial for larval growth and development, however, when nutrients are abundant, the presence of microbiota is detrimental. Storelli et al.18 found that in the absence of yeast, the symbiotic bacteria Lactobacillus plantarum in the gut of Drosophila plays a role in upstream gene regulation of the TOR-dependent host nutrient-sensing system that controls hormone growth signals, demonstrating that the microbial community of Drosophila promotes the growth of larvae in nutrient deficient conditions. Other studies have also investigated the promoting effect of L. plantarum on the growth of Drosophilaunder malnutrition conditions32. These findings are consistent with the present research that showed that E. casseliflavus has a nutrition-dependent effect on the life history traits of S. frugiperda.Insects and their enteric microbiota have established an interdependent symbiotic relationship over a long period of evolution, which is crucial for the survival and adaptability of insects33. The loss of important enteric microbiota in insects may have a significant impact on the host insect. For example, when antibiotics are used to treat the larvae of Plutella xylostella, the mortality rate of the larvae increases, pupal weight decreases, and deformities may even occur. The primary reason behind these negative impacts may be the removal of beneficial enteric bacteria, which disrupt the ecological balance of microorganisms in the intestine and impair its digestive function, resulting in a series of adverse effects34. Likewise, when antibiotic treatment was applied to S. frugiperda larvae, the food intake (body weight positively correlated with food intake) of the antibiotic treatment group was significantly lower than that of the control group, and the larval stage of S. frugiperdain the antibiotic treatment group was significantly longer than that of the control group35.Research showed that the enteric microbiota can modulate various biological processes by influencing the expression of insect-related genes36. Previous studies have indicated that carbohydrates can provide energy during catabolic processes37. Treatment of Bombyx moriwith afidopyropen resulted in significant down-regulation of genes associated with carbohydrate energy metabolism and the immune system, leading to significant reductions in growth, development, and vitality38. Another study found that mutualistic partners of the red turpentine beetle Dendroctonus valens LeConte, namely the mutualistic fungi Leptographium procerum and symbiotic bacteria such as Erwinia and Serratia, degrade deterrent pine carbohydrates like D-pinitol, thus leaving more D-glucose available to enhance the adaptability of D. valens39. Our study demonstrates that treatment of larvae with E. casseliflavus significantly impairs carbohydrate transport and metabolism, with 61 genes exhibiting differential expression, of which 58 were significantly downregulated (Fig. 7A). This further impacts energy metabolism, suggesting a negative regulatory role in the growth and development of S. frugiperda larvae.In E. casseliflavus group, KEGG pathway analysis revealed that numerous genes involved in physiological metabolism were downregulated, such as those related to carbon metabolism, starch and sucrose metabolism, and galactose metabolism (Fig. 9A). Notably, genes such as glycogen phosphorylase (gene-LOC118265182, Log2 FC=−1.76), UDP-glycosyltransferase UGT5 (gene-LOC118279189, Log2 FC=−6.80), and maltase 2 (gene-LOC118273028, Log2 FC=−2.78) were significantly downregulated. Starch is a high molecular weight carbohydrate, and the loss of starch-degrading enzyme genes leads to growth defects in L. procerum and D. valenslarvae. Notably, ammonia released by red turpentine beetle-associated bacteria can activate starch conversion into a carbon source (glucose), thereby supplementing the growth of red turpentine beetle larvae and alleviating nutrient limitation40. After host transfer, the adaptability of Bemisia tabaciAsia II 3 was lower than that of MEAM1, with most genes in Asia II 3 being downregulated, including those involved in glycolysis, pyruvate metabolism, the TCA cycle, and oxidative phosphorylation, significantly inhibiting carbohydrate and energy metabolism pathways41. Silencing of UDP-glycosyltransferase genes in S. frugiperdalarvae significantly inhibits their growth10,42.Amino acids play a crucial role in controlling physiological metabolism and development43, and have been shown to promote insect larval growth and cell proliferation44. Additionally, amino acids are essential in regulating the growth and reproduction of host Drosophila45,46. Imbalances in amino acid levels can induce rapid and reversible activation of three DA neurons in Drosophilalarvae, thereby influencing their food intake47. Previous studies have indicated that afidopyropen inhibits the growth and silk protein synthesis of the silkworm by suppressing phosphoserine aminotransferase 1 and vitamin B6 metabolism38. Notably, insect hormones play a critical role in regulating biological processes. In Helicoverpa armigera, the steroid hormone 20E reprograms carbohydrate and amino acid metabolism by modulating the expression of different genes, thereby maintaining glucose homeostasis during metamorphosis and supporting insect development44. Our study found that genes related to amino acid biosynthesis, tyrosine metabolism, alanine and proline metabolism, and insect hormone biosynthesis were downregulated, which is consistent with the reduced fitness of S. frugiperda larvae in the E. casseliflavus group. In contrast, the E. mundtii group showed minimal changes in genes related to energy metabolism, corresponding to its insignificant impact on the growth and development of S. frugiperda larvae.In summary, this study found that E. casseliflavus has a nutrient-dependent effect on life history traits, while E. mundtii has no significant impact on the developmental performance of S. frugiperda. Transcriptomic analysis revealed a significant decrease in differentially expressed genes related to carbohydrate transport and physiological metabolism in the E. casseliflavus group, which may aid in further elucidating the molecular mechanisms regulating the growth and development of S. frugiperda (Fig. 10).Fig. 10Graphical abstract.Full size image
Data availability
Raw sequencing reads have been deposited in the NCBI Sequence Read Archive (SRA) database under accession number PRJNA 1187672 but access to these data is restricted. The data will be made publicly available one year after publication.The datasets generated during and/or analysed during the current study are available from the corresponding author on reasonable request.
ReferencesGao, H. H. et al. Effects of nutrition on the development and gut microbial community structure of Drosophila Suzukii (Diptera: Drosophilidae). Acta Entomologica Sinica. 1–12. https://doi.org/10.16380/j.kcxb.2023.10.010 (2023).Acevedo, F. E. et al. Fall armyworm-associated gut bacteria modulate plant defense responses. Mol. Plant-Microbe Interactions: MPMI. 30 (2), 127–137. https://doi.org/10.1094/MPMI-11-16-0240-R (2017).Article
CAS
PubMed
Google Scholar
Muhammad, A., Habineza, P., Ji, T., Hou, Y. & Shi, Z. Intestinal microbiota confer protection by priming the immune system of red palm weevil Rhynchophorus ferrugineus Olivier (Coleoptera: Dryophthoridae). Front. Physiol. 10, 1303. https://doi.org/10.3389/fphys.2019.01303 (2019).Article
PubMed
PubMed Central
Google Scholar
Xia, X. et al. Gut microbiota mediate insecticide resistance in the Diamondback moth, Plutella Xylostella (L). Front. Microbiol. 9, 25. https://doi.org/10.3389/fmicb.2018.00025 (2018).Article
PubMed
PubMed Central
MATH
Google Scholar
Lee, J., Han, G., Kim, J. W., Jeon, C. O. & Hyun, S. Taxon-specific effects of Lactobacillus on Drosophila host development. Microb. Ecol. 79 (1), 241–251. https://doi.org/10.1007/s00248-019-01404-9 (2020).Article
ADS
PubMed
MATH
Google Scholar
Zheng, H., Powell, J. E., Steele, M. I., Dietrich, C. & Moran, N. A. Honeybee gut microbiota promotes host weight gain via bacterial metabolism and hormonal signaling. Proc. Natl. Acad. Sci. U.S.A. 114 (18), 4775–4780. https://doi.org/10.1073/pnas.1701819114 (2017).Article
ADS
CAS
PubMed
PubMed Central
Google Scholar
Raza, M. F. et al. Gut microbiota promotes host resistance to low-temperature stress by stimulating its arginine and proline metabolism pathway in adult Bactrocera dorsalis. PLoS Pathog. 16 (4), e1008441. https://doi.org/10.1371/journal.ppat.1008441 (2020).Article
CAS
PubMed
PubMed Central
Google Scholar
Iatsenko, I., Boquete, J. P. & Lemaitre, B. Microbiota-derived lactate activates production of reactive oxygen species by the intestinal NADPH oxidase nox and shortens Drosophila lifespan. Immunity 49 (5), 929–942e5. https://doi.org/10.1016/j.immuni.2018.09.017 (2018).Article
CAS
PubMed
Google Scholar
Wang, P. et al. Host selection and adaptation of the invasive pest Spodoptera Frugiperda to indica and Japonica rice cultivars. Entomol. Generalis. 42 (3), 403–411. https://doi.org/10.1127/entomologia/2022/1330 (2022).Article
CAS
MATH
Google Scholar
Han, W. K., Tang, F. X., Yan, Y. Y., Wang, Y. & Liu, Z. W. Plasticity of the gene transcriptional level and microbiota in the gut contributes to the adaptability of the fall armyworm to rice plants. J. Agric. Food Chem. 71 (47), 18546–18556. https://doi.org/10.1021/acs.jafc.3c05506 (2023).Article
CAS
PubMed
Google Scholar
Xu, S. et al. The threat of the fall armyworm to Asian rice production is amplified by the brown planthopper. Plant. Cell. Environ. https://doi.org/10.1111/pce.15194 (2024). Advance online publication.Article
PubMed
PubMed Central
Google Scholar
Jones, A. G., Mason, C. J., Felton, G. W. & Hoover, K. Host plant and population source drive diversity of microbial gut communities in two polyphagous insects. Sci. Rep. 9 (1), 2792. https://doi.org/10.1038/s41598-019-39163-9 (2019).Article
ADS
CAS
PubMed
PubMed Central
Google Scholar
Wang, P., He, P. C., Fu, W. D. & Chu, D. Adverse effects of high concentrations of two enteric bacteria on Spodoptera Frugiperda and their benefits with respect to insect food quality. Entomol. Generalis, 43(4): 839–847. https://doi.org/10.1127/entomologia/2023 /2019 (2023).Fu, J. et al. Composition and diversity of gut microbiota across developmental stages of Spodoptera Frugiperda and its effect on the reproduction. Front. Microbiol. 14, 1237684. https://doi.org/10.3389/fmicb.2023.1237684 (2023).Article
PubMed
PubMed Central
Google Scholar
Jeon, J. et al. Spodoptera Frugiperda (Lepidoptera: Noctuidae) life table comparisons and gut Microbiome analysis reared on corn varieties. Insects 14 (4), 358. https://doi.org/10.3390/insects14040358 (2023).Article
PubMed
PubMed Central
MATH
Google Scholar
Gomes, A. F. F., de Almeida, L. G. & Cônsoli, F. L. Comparative genomics of pesticide-degrading Enterococcus symbionts of Spodoptera Frugiperda (Lepidoptera: Noctuidae) leads to the identification of two new species and the reappraisal of insect-associated Enterococcus species. Microb. Ecol. 86 (4), 2583–2605. https://doi.org/10.1007/s00248-023-02264-0 (2023).Article
ADS
CAS
PubMed
Google Scholar
Almeida, L. G., Moraes, L. A., Trigo, J. R., Omoto, C. & Cônsoli, F. L. The gut microbiota of insecticide-resistant insects houses insecticide-degrading bacteria: A potential source for biotechnological exploitation. PLoS One. 12 (3), e0174754. https://doi.org/10.1371/journal.pone.0174754 (2017).Article
CAS
PubMed
PubMed Central
Google Scholar
Storelli, G. et al. Lactobacillus plantarum promotes Drosophila systemic growth by modulating hormonal signals through TOR-dependent nutrient sensing. Cell Metabol. 14 (3), 403–414. https://doi.org/10.1016/j.cmet.2011.07.012 (2011).Article
CAS
Google Scholar
Chen, S., Geng, P., Xiao, Y. & Hu, M. Bioremediation of β-cypermethrin and 3-phenoxybenzaldehyde contaminated soils using Streptomyces aureus HP-S-01. Appl. Microbiol. Biotechnol. 94 (2), 505–515. https://doi.org/10.1007/s00253-011-3640-5 (2012).Article
CAS
PubMed
Google Scholar
Kanehisa, M. & Goto, S. KEGG: Kyoto encyclopedia of genes and genomes. Nucleic Acids Res. 28, 27–30. https://doi.org/10.1093/nar/28.1.27 (2000).Article
CAS
PubMed
PubMed Central
MATH
Google Scholar
Kanehisa, M., Furumichi, M., Sato, Y., Matsuura, Y. & Ishiguro-Watanabe, M. KEGG: biological systems database as a model of the real world. Nucleic Acids Res. 53, D672–D677. https://doi.org/10.1093/nar/gkae909 (2025).Article
PubMed
Google Scholar
Li, D. D., Li, J. Y., Hu, Z. Q., Liu, T. X. & Zhang, S. Z. Fall armyworm gut bacterial diversity associated with different developmental stages, environmental habitats, and diets. Insects 13 (9), 762. https://doi.org/10.3390/insects13090762 (2022).Article
PubMed
PubMed Central
MATH
Google Scholar
de Diego-Diaz, B. et al. Genome sequence of Enterococcus mundtii EM01, isolated from Bombyx Mori midgut and responsible for flacherie disease in silkworms reared on an artificial diet. Genome Announcements. 6 (3), e01495–e01417. https://doi.org/10.1128/genomeA.01495-17 (2018).Article
PubMed
PubMed Central
Google Scholar
Grau, T., Vilcinskas, A. & Joop, G. Probiotic Enterococcus mundtii isolate protects the model insect tribolium castaneum against Bacillus Thuringiensis. Front. Microbiol. 8, 1261. https://doi.org/10.3389/fmicb.2017.01261 (2017).Article
PubMed
PubMed Central
Google Scholar
Thakur, A., Dhammi, P., Saini, H. S. & Kaur, S. Pathogenicity of bacteria isolated from gut of Spodoptera Litura (Lepidoptera: Noctuidae) and fitness costs of insect associated with consumption of bacteria. J. Invertebr. Pathol. 127, 38–46. https://doi.org/10.1016/j.jip.2015.02.007 (2015).Article
PubMed
Google Scholar
Lan, B. M. Diversity and function of gut bacterial symbions of Spodoptera litura (Fujian Agriculture and Forestry University, 2016).MATH
Google Scholar
Zhang, N. et al. Contribution of sample processing to gut Microbiome analysis in the model lepidoptera, silkworm Bombyx Mori. Comput. Struct. Biotechnol. J. 19, 4658–4668. https://doi.org/10.1016/j.csbj.2021.08.020 (2021).Article
CAS
PubMed
PubMed Central
MATH
Google Scholar
Chen, B. et al. Biodiversity and activity of the gut microbiota across the life history of the insect herbivore Spodoptera littoralis. Sci. Rep. 6, 29505. https://doi.org/10.1038/srep29505 (2016).Article
ADS
CAS
PubMed
PubMed Central
Google Scholar
Kumar, D. et al. Study of gut bacterial diversity of Bombyx Mandarina and Bombyx Mori through 16S rRNA gene sequencing. J. Asia. Pac. Entomol. 22 (2), 522–530. https://doi.org/10.1016/j.aspen.2019.03.005 (2019).Article
MATH
Google Scholar
Mason, C. J., Peiffer, M., Chen, B., Hoover, K. & Felton, G. W. Opposing growth responses of lepidopteran larvae to the establishment of gut microbiota. Microbiol. Spectr. 10 (4), e0194122. https://doi.org/10.1128/spectrum.01941-22 (2022).Article
CAS
PubMed
Google Scholar
Cai, Z. H. The effects of gut microbiota on the growth and the repair of irradiated damage in Bactrocera dorsalis. Huazhong Agricultural University. Doi: 10.27158/d. cnki. ghznu. 000906 (2020).Matos, R. C. et al. D-Alanylation of teichoic acids contributes to Lactobacillus plantarum-mediated Drosophila growth during chronic undernutrition. Nat. Microbiol. 2 (12), 1635–1647. https://doi.org/10.1038/s41564-017-0038-x (2017).Article
CAS
PubMed
PubMed Central
MATH
Google Scholar
Gupta, A. & Nair, S. Dynamics of insect-microbiome interaction influence host and microbial symbiont. Front. Microbiol. 11, 1357. https://doi.org/10.3389/fmicb.2020.01357 (2020).Article
PubMed
PubMed Central
MATH
Google Scholar
Lin, X. L., Kang, Z. W., Pan, Q. J. & Liu, T. X. Evaluation of five antibiotics on larval gut bacterial diversity of Plutella Xylostella (Lepidoptera: Plutellidae). Insect Sci. 22 (5), 619–628. https://doi.org/10.1111/1744-7917.12168 (2015).Article
CAS
PubMed
MATH
Google Scholar
Lü, D. et al. Dynamics of gut microflora across the life cycle of Spodoptera Frugiperda and its effects on the feeding and growth of larvae. Pest Manag. Sci. 79 (1), 173–182. https://doi.org/10.1002/ps.7186 (2023).Article
ADS
CAS
PubMed
MATH
Google Scholar
Broderick, N. A., Buchon, N. & Lemaitre, B. Microbiota-induced changes in drosophila melanogaster host gene expression and gut morphology. mBio 5 (3), e01117–e01114. https://doi.org/10.1128/mBio.01117-14 (2014).Article
CAS
PubMed
PubMed Central
Google Scholar
Dashty, M. A quick look at biochemistry: carbohydrate metabolism. Clin. Biochem. 46 (15), 1339–1352. https://doi.org/10.1016/j.clinbiochem.2013.04.027 (2013).Article
CAS
PubMed
MATH
Google Scholar
Wei, E. et al. Afidopyropen suppresses silkworm growth and vitality by affecting carbohydrate metabolism and immune function. Pestic. Biochem. Physiol. 195, 105568. https://doi.org/10.1016/j.pestbp.2023.105568 (2023).Article
CAS
PubMed
MATH
Google Scholar
Liu, F. et al. Symbiotic microbes aid host adaptation by metabolizing a deterrent host pine carbohydrate d-pinitol in a beetle-fungus invasive complex. Sci. Adv. 8 (51), eadd5051. https://doi.org/10.1126/sciadv.add5051 (2022).Article
CAS
PubMed
PubMed Central
Google Scholar
Liu, F., Wickham, J. D., Cao, Q., Lu, M. & Sun, J. An invasive beetle-fungus complex is maintained by fungal nutritional-compensation mediated by bacterial volatiles. ISME J. 14 (11), 2829–2842. https://doi.org/10.1038/s41396-020-00740-w (2020).Article
CAS
PubMed
PubMed Central
Google Scholar
Xu, H. X. et al. Transcriptional responses of invasive and Indigenous whiteflies to different host plants reveal their disparate capacity of adaptation. Sci. Rep. 5, 10774. https://doi.org/10.1038/srep10774 (2015).Article
ADS
CAS
PubMed
PubMed Central
MATH
Google Scholar
Israni, B. et al. The fall armyworm Spodoptera Frugiperda utilizes specific UDP-glycosyltransferases to inactivate maize defensive benzoxazinoids. Front. Physiol. 11, 604754. https://doi.org/10.3389/fphys.2020.604754 (2020).Article
PubMed
PubMed Central
Google Scholar
Manière, G., Alves, G., Berthelot-Grosjean, M. & Grosjean, Y. Growth regulation by amino acid transporters in drosophila larvae. Cell. Mol. Life Sci. 77 (21), 4289–4297. https://doi.org/10.1007/s00018-020-03535-6 (2020).Article
CAS
PubMed
PubMed Central
MATH
Google Scholar
44. Wang, X. P. 20-Hydroxyecdysone reprogrammes glucose and amino acidmetabolism to regulate insect metamorphosis.Shandong University, PhD dissertation.doi:10.27272/d.cnki.gshdu.2023.000303 (2023).Hoedjes, K. M., Rodrigues, M. A. & Flatt, T. Amino acid modulation of lifespan and reproduction in drosophila. Curr. Opin. Insect Sci. 23, 118–122. https://doi.org/10.1016/j.cois.2017.07.005 (2017).Article
PubMed
MATH
Google Scholar
Leitão-Gonçalves, R. et al. Commensal bacteria and essential amino acids control food choice behavior and reproduction. PLoS Biol. 15 (4), e2000862. https://doi.org/10.1371/journal.pbio.2000862 (2017).Article
CAS
PubMed
PubMed Central
Google Scholar
Bjordal, M., Arquier, N., Kniazeff, J., Pin, J. P. & Léopold, P. Sensing of amino acids in a dopaminergic circuitry promotes rejection of an incomplete diet in drosophila. Cell 156 (3), 510–521. https://doi.org/10.1016/j.cell.2013.12.024 (2014).Article
CAS
PubMed
Google Scholar
Download referencesAcknowledgementsThis research was supported by the TaiShan Scholar Foundation of Shandong Province of China (tstp 20221135), the Shandong Modern Agricultural Technology & Industry System (SDAIT-17-07), and the Qingdao Agricultural University High-level Talent Fund (663-1121027).Author informationAuthor notesWendou Fu and Peng Wang contributed equally.Authors and AffiliationsShandong Engineering Research Center for Environment-Friendly Agricultural Pest Management, College of Plant Health and Medicine, Qingdao Agricultural University, Qingdao, 266109, P. R. ChinaWendou Fu, Peng Wang, Peicong He & Dong ChuShandong Province Centre for Bioinvasions and Eco-Security, Qingdao, 266109, P. R. ChinaWendou Fu, Peng Wang, Peicong He & Dong ChuAuthorsWendou FuView author publicationsYou can also search for this author inPubMed Google ScholarPeng WangView author publicationsYou can also search for this author inPubMed Google ScholarPeicong HeView author publicationsYou can also search for this author inPubMed Google ScholarDong ChuView author publicationsYou can also search for this author inPubMed Google ScholarContributionsD.C. and P.W. designed the project. W.F. and P.H. performed the experiments and analyzed the data. W.F. and P.W. wrote the main manuscript text. All authors reviewed the manuscript.Corresponding authorCorrespondence to
Dong Chu.Ethics declarations
Competing interests
The authors declare no competing interests.
Informed consent
We hereby attest that we have informed consent from all persons figuring in images included in this.
manuscript to be shown in online open-access publications.
Additional informationPublisher’s noteSpringer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.Electronic supplementary materialBelow is the link to the electronic supplementary material.Supplementary Material 1Rights and permissions
Open Access This article is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License, which permits any non-commercial use, sharing, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if you modified the licensed material. You do not have permission under this licence to share adapted material derived from this article or parts of it. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by-nc-nd/4.0/.
Reprints and permissionsAbout this articleCite this articleFu, W., Wang, P., He, P. et al. Distinct effects of two dominant enteric bacteria on the developmental performance of spodoptera frugiperda and their association with physiological metabolism.
Sci Rep 15, 10509 (2025). https://doi.org/10.1038/s41598-025-95296-0Download citationReceived: 13 November 2024Accepted: 20 March 2025Published: 27 March 2025DOI: https://doi.org/10.1038/s41598-025-95296-0Share this articleAnyone you share the following link with will be able to read this content:Get shareable linkSorry, a shareable link is not currently available for this article.Copy to clipboard
Provided by the Springer Nature SharedIt content-sharing initiative
Keywords
Spodoptera frugiperda
Enteric bacteria
Enterococcus mundtii
Enterococcus casseliflavus
Life history traitPhysiological metabolism