Evolutionary ecology of beta‐lactam gene clusters in animals

Suring, Wouter; Meusemann, Karen; Blanke, Alexander; Mariën, Janine; Schol, Tim; Agamennone, Valeria; Faddeeva-Vakhrusheva, Anna; Berg, Matty P.; Brouwer, Abraham; Straalen, Nico M. van; Roelofs, Dick

doi:10.1111/mec.14109

Cited by 26 publications

(40 citation statements)

References 57 publications

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“…Genome annotation and b-lactam ELISA analysis suggest that the F. candida host is able to synthesize a penicillinlike antibiotic (Suring et al, 2017). Thus, colonization of F. candida's gut by Bacillus VU-DES13 will only be successful, if the strain can withstand b-lactam (penicillinlike) antibiotic exposure from the host.…”

Section: Antibiotic Resistancementioning

confidence: 99%

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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Section: Antibiotic Resistancementioning

confidence: 99%

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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“…Indeed, three of four analysed species from the springtail order Symphypleona do not possess these genes (Suring et al, 2017). It is surprising however, that we did not find evidence of these genes in the genome if D. tigrina, which inhabits soils and likely needs to cope with high microbial load.…”

Section: Genomesmentioning

confidence: 64%

“…'uncharacterized protein' (for proteins with hits without annotations). Collembola are considered the only known animal group that might be able of antibiotic synthesis through the horizontal transfer of beta-lactam gene clusters from soil fungi (Faddeeva-Vakhrusheva et al, 2017;Suring et al, 2017). We searched the genomes for genes homologous of the isopenicillin N synthase-like gene found in F. candida by querying the nucleotide sequence of the mRNA (NCBI accession XM_022089550.1) using blastn and DIAMOND blastx against the genome assembly (Buchfink, Xie & Huson, 2015).…”

Section: Assemblies Assessmentmentioning

confidence: 99%

“…It is surprising however, that we did not find evidence of these genes in the genome if D. tigrina, which inhabits soils and likely needs to cope with high microbial load. Suring et al (2017) identified beta-lactam gene clusters in four of six Entomobryomorpha species they investigated, including F. candida, which belongs to the same family as D. tigrina (Isotomidae). Beta-lactam gene clusters are sometimes not recovered from the genomes of hemiedaphic species (Suring et al, 2017), and D. tigrina also belongs to this group (Potapov, 2001).…”

Section: Genomesmentioning

confidence: 99%

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Biodiversity genomics of small metazoans: high qualityde novogenomes from single specimens of field-collected and ethanol-preserved springtails

Schneider

Woehle

Greve

et al. 2020

Preprint

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Genome sequencing of all known eukaryotes on Earth promises unprecedented advances in evolutionary sciences, ecology, systematics and in biodiversity-related applied fields such as environmental management and natural product research. Advances in DNA sequencing technologies make genome sequencing feasible for many non-genetic model species. However, genome sequencing today relies on large quantities of high quality, high molecular weight (HMW) DNA which is mostly obtained from fresh tissues. This is problematic for biodiversity genomics of Metazoa as most species are small and yield minute amounts of DNA. Furthermore, briging living specimens to the lab bench not realistic for the majority of species. Here we overcome those difficulties by sequencing two species of springtails (Collembola) from single specimens preserved in ethanol. We used a newly developed, genome-wide amplification-based protocol to generate PacBio libraries for HiFi long-read sequencing. The assembled genomes were highly continuous. They can be considered complete as we recovered over 95% of BUSCOs. Genome-wide amplification does not seem to bias genome recovery. Presence of almost complete copies of the mitochondrial genome in the nuclear genome were pitfalls for automatic assemblers. The genomes fit well into an existing phylogeny of springtails. A neotype is designated for one of the species, blending genome sequencing and creation of taxonomic references. Our study shows that it is possible to obtain high quality genomes from small, field-preserved sub-millimeter metazoans, thus making their vast diversity accessible to the fields of genomics.

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“…Beta-lactamases are a priori useless for giant viruses, which are grown in the presence of various antibiotics, including beta-lactams 24 , but our findings enhance the recent reconsideration of the function of MBL fold proteins. Thus, the recent description of penicillin secretion by arthropods 25 and the demonstration of active beta-lactamase in vertebrates including humans 19 , as well as in archaea 6 and fungi 26 show that MBL fold proteins have a dramatically broad distribution. In humans, 18 genes were annotated as beta-lactamases, whose activity had not been biologically-tested until recently 19 .…”

Section: Discussionmentioning

confidence: 99%

A metallo-beta-lactamase with both beta-lactamase and ribonuclease activity is linked with traduction in giant viruses

Colson

Pinault

Azza

et al. 2019

Preprint

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25Enzymatic proteins with a metallo-beta-lactamase (MBL) fold have been essentially studied 26 in bacteria for their activity on beta-lactam antibiotics. However, the MBL fold is ancient and 27 highly conserved, and these proteins are capable of cleaving a broad range of substrates. It has 28 recently been shown that MBLs are present in a wide array of cellular organisms, including 29 eukaryotes and archaea. We show here that Tupanvirus deep ocean, a giant virus, also 30 encodes a protein with a MBL fold. Phylogeny showed its clustering with transfer 31 ribonucleases (RNases) and the presence of orthologs in other giant viruses, mainly those 32 harboring the largest sets of translation components. In addition, it suggests an ancient origin 33 for these genes and a transfer between giant viruses and Acanthamoeba spp., a host of many 34 giant viruses. Biologically, after its expression in Escherichia coli, the tupanvirus protein was 35 found to hydrolyse nitrocefin, a chromogenic beta-lactam. We also observed an hydrolysis of 36 penicillin G (10 µg/mL) and detected the metabolite of penicillin G hydrolysis, 37 benzylpenilloic acid. This was inhibited by sulbactam, a beta-lactamase inhibitor. In addition, 38we tested the degradation of single-stranded DNA, double-stranded DNA, and RNAs, and 39 observed a strong activity on RNAs from seven bacteria with G+C varying from 42% to 67%, 40 and from Acanthamoeba castellanii, the tupanvirus host. This was not inhibited by sulbactam 41 or ceftriaxone. RNase activity was estimated to be 0.45±0.15 mU/mg using a fluorescence-42 based assay. Our results still broaden the range of hosts of MBL fold proteins and 43 demonstrate that such protein can have dual beta-lactamase/nuclease activities. We suggest 44 that they should be annotated according to this finding to avoid further confusion. 45 46 3 TEXT 47 48

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Evolutionary ecology of beta‐lactam gene clusters in animals

Cited by 26 publications

References 57 publications

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

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

Biodiversity genomics of small metazoans: high qualityde novogenomes from single specimens of field-collected and ethanol-preserved springtails

A metallo-beta-lactamase with both beta-lactamase and ribonuclease activity is linked with traduction in giant viruses

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