The microbiome of<i>Folsomia candida</i>: an assessment of bacterial diversity in a<i>Wolbachia</i>-containing animal

Agamennone, Valeria; Jakupović, Dennis; Weedon, James T.; Suring, Wouter; Straalen, Nico M. van; Roelofs, Dick; Röling, Wilfred F. M.

doi:10.1093/femsec/fiv128

Cited by 33 publications

(44 citation statements)

References 43 publications

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“…A detailed characterization of the microbiome of F. candida has recently been reported, enabling further studies on interactions between its beta‐lactam genes and the bacterial community in the gut (Agamennone et al . ).…”

Section: Resultsmentioning

confidence: 97%

Evolutionary ecology of beta‐lactam gene clusters in animals

et al. 2017

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Beta-lactam biosynthesis was thought to occur only in fungi and bacteria, but we recently reported the presence of isopenicillin N synthase in a soil-dwelling animal, Folsomia candida. However, it has remained unclear whether this gene is part of a larger beta-lactam biosynthesis pathway and how widespread the occurrence of penicillin biosynthesis is among animals. Here, we analysed the distribution of beta-lactam biosynthesis genes throughout the animal kingdom and identified a beta-lactam gene cluster in the genome of F. candida (Collembola), consisting of isopenicillin N synthase (IPNS), δ-(L-α-aminoadipoyl)-L-cysteinyl-D-valine synthetase (ACVS), and two cephamycin C genes (cmcI and cmcJ) on a genomic scaffold of 0.76 Mb. All genes are transcriptionally active and are inducible by stress (heat shock). A beta-lactam compound was detected in vivo using an ELISA beta-lactam assay. The gene cluster also contains an ABC transporter which is coregulated with IPNS and ACVS after heat shock. Furthermore, we show that different combinations of beta-lactam biosynthesis genes are present in over 60% of springtail families, but they are absent from genome- and transcript libraries of other animals including close relatives of springtails (Protura, Diplura and insects). The presence of beta-lactam genes is strongly correlated with an euedaphic (soil-living) lifestyle. Beta-lactam genes IPNS and ACVS each form a phylogenetic clade in between bacteria and fungi, while cmcI and cmcJ genes cluster within bacteria. This suggests a single horizontal gene transfer event most probably from a bacterial host, followed by differential loss in more recently evolving species.

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Section: Resultsmentioning

confidence: 97%

Evolutionary ecology of beta‐lactam gene clusters in animals

et al. 2017

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“…A previous study based on cloning and 16S rRNA gene sequencing isolated 95 clones from the springtail, 83 of which (87%) were identified as Bacillus weihenstephaniensis Lechner et al (Czarnetzki & Tebbe, 2004). Agamennone et al (2015) also indicated that members of the B. cereus group are among the dominant groups in F. candida microbiome, representing 4% of the reads in a natural population of springtails. However, the limited resolution of 16S rRNA in this clade did not allow for a more specific identification within this clade.…”

Section: Discussionmentioning

confidence: 99%

“…Agamennone et al. () also indicated that members of the B. cereus group are among the dominant groups in F. candida microbiome, representing 4% of the reads in a natural population of springtails. However, the limited resolution of 16S rRNA in this clade did not allow for a more specific identification within this clade.…”

Section: Discussionmentioning

confidence: 99%

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Genome annotation and antimicrobial properties of Bacillus toyonensis VU‐DES13, isolated from the Folsomia candida gut

Agamennone¹,

Straalen

Brouwer³

et al. 2019

Entomologia Exp Applicata

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Antibiotic resistance necessitates the search for new bioactive compounds with novel mechanisms of action. Natural products derived from bacteria and fungi are widely used in the field of medicine and new environments can be explored as sources of antimicrobials. Bacteria associated with springtails have shown high inhibitory activity against pathogens. Here, we characterized a bacterial strain with high potential for antimicrobial activity, isolated from the gut of the springtail Folsomia candida Willem (Collembola: Isotomidae). The strain was characterized using the ‘analytical profile index’ and the ‘minimal inhibitory concentration’ assay to test for antibiotic resistance. Agar overlay and agar disk diffusion assays were used to test the inhibitory activity of the strain and its extract against a variety of pathogens, and reporter assays were used to investigate the mode of action. High‐performance liquid chromatography was used to analyze and fractionate the extract of bacterial culture, followed by additional assays on the fractions. The genome of the strain was screened for presence of antibiotic resistance genes and secondary metabolite gene clusters. The isolate was identified as Bacillus toyonensis Jiménez et al., but it displayed differences in metabolic profile when compared to the type species. The isolate was highly resistant to penicillin and inhibited the growth of a variety of pathogenic microorganisms. Genome analysis revealed an enrichment of resistance genes for β‐lactam antibiotics compared to the type isolate. Also, secondary metabolite clusters involved in the production of siderophores, bacteriocins, and nonribosomal peptide synthetases were identified. In conclusion, a unique Bacillus strain was isolated from the gut of F. candida, for which we provide evidence of inhibitory activity against an array of pathogens. This, coupled with high resistance to penicillin as substantiated by the presence of resistance genes, points to the potential of B. toyonensis VU‐DES13 to provide a new source of antimicrobial compounds.

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“…The host’s genome contains biosynthetic gene clusters for secondary metabolites, such as for β-lactams (2), which are induced in the gut epithelium upon stress (3). Previous amplicon-sequencing studies (4, 5) revealed the prominence of B. cereus in the F. candida midgut. An association between the propagation cycle of members of the B. cereus clade and the internal environment of animals has been suggested (6, 7).…”

Section: Genome Announcementmentioning

confidence: 94%

Draft Genome Sequence of Bacillus toyonensis VU-DES13, Isolated from Folsomia candida ( Collembola : Entomobryidae )

Janssens

Boer²,

Agamennone

et al. 2017

Genome Announc

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We present here the draft genome of Bacillus toyonensis VU-DES13, which was isolated from the midgut of the soil-living springtail Folsomia candida. Previous research revealed the presence of gene clusters for the biosynthesis of various secondary metabolites, including β-lactam antibiotics, in the host's genome. The genome data are discussed in the light of the antimicrobial properties against fungi and oomycetes and a high level of β-lactam resistance of the isolate.

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The microbiome ofFolsomia candida: an assessment of bacterial diversity in aWolbachia-containing animal

Cited by 33 publications

References 43 publications

Evolutionary ecology of beta‐lactam gene clusters in animals

Evolutionary ecology of beta‐lactam gene clusters in animals

Genome annotation and antimicrobial properties of Bacillus toyonensis VU‐DES13, isolated from the Folsomia candida gut

Draft Genome Sequence of Bacillus toyonensis VU-DES13, Isolated from Folsomia candida ( Collembola : Entomobryidae )

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