Genome Sequence of Streptomyces griseus Strain XylebKG-1, an Ambrosia Beetle-Associated Actinomycete

Grubbs, Kirk J.; Biedermann, Peter H. W.; Suen, Garret; Adams, Sandra M.; Moeller, Joseph A.; Klassen, Jonathan L.; Goodwin, Lynne; Woyke, Tanja; Munk, A. Christine; Bruce, David; Detter, Chris; Tapia, Roxanne; Han, Cliff; Currie, Cameron R.

doi:10.1128/jb.00330-11

Cited by 25 publications

(20 citation statements)

References 19 publications

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“…In Dendroctonus bark beetles, several bacterial groups have been found to reduce the growth of antagonistic fungi (Scott et al, 2008), and some of them are actively applied with oral secretions during specialized cleaning behaviours by the adults (Cardoza et al, 2006). Streptomyces griseus, which is known to produce antibiotics, has been recently isolated from X. saxesenii galleries (Grubbs et al, 2011). Whether and how bacteria influence the composition of ambrosia gardens remains to be investigated.…”

Section: Fungus Dynamics In a Laboratory Setting Vs Field Galleriesmentioning

confidence: 99%

Abundance and dynamics of filamentous fungi in the complex ambrosia gardens of the primitively eusocial beetleXyleborinus saxeseniiRatzeburg (Coleoptera: Curculionidae, Scolytinae)

Biedermann

Klepzig

Taborsky

et al. 2012

FEMS Microbiol Ecol

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Insect fungus gardens consist of a community of interacting microorganisms that can have either beneficial or detrimental effects to the farmers. In contrast to fungus-farming ants and termites, the fungal communities of ambrosia beetles and the effects of particular fungal species on the farmers are largely unknown. Here, we used a laboratory rearing technique for studying the filamentous fungal garden community of the ambrosia beetle, Xyleborinus saxesenii, which cultivates fungi in tunnels excavated within dead trees. Raffaelea sulfurea and Fusicolla acetilerea were transmitted in spore-carrying organs by gallery founding females and established first in new gardens. Raffaelea sulfurea had positive effects on egg-laying and larval numbers. Over time, four other fungal species emerged in the gardens. Prevalence of one of them, Paecilomyces variotii, correlated negatively with larval numbers and can be harmful to adults by forming biofilms on their bodies. It also comprised the main portion of garden material removed from galleries by adults. Our data suggest that two mutualistic, several commensalistic and one to two pathogenic filamentous fungi are associated with X. saxesenii. Fungal diversity in gardens of ambrosia beetles appears to be much lower than that in gardens of fungus-culturing ants, which seems to result from essential differences in substrates and behaviours.

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Section: Fungus Dynamics In a Laboratory Setting Vs Field Galleriesmentioning

confidence: 99%

Abundance and dynamics of filamentous fungi in the complex ambrosia gardens of the primitively eusocial beetleXyleborinus saxeseniiRatzeburg (Coleoptera: Curculionidae, Scolytinae)

Biedermann

Klepzig

Taborsky

et al. 2012

FEMS Microbiol Ecol

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“…The genome of S. griseus XylebKG-1 has previously been sequenced [48] allowing us to generate a genome based phylogeny for this isolate. Proteins from all complete Streptomyces genomes were predicted using prodigal [59] for consistency and annotated using HMMer [60] models generated from KEGG [61] gene families, of which 1,364 KEGG gene families were conserved in all genomes.…”

Section: Methodsmentioning

confidence: 99%

“…Active compounds were isolated using bioassay-guided HPLC fractionation, chemically characterized using NMR spectroscopy and mass spectrometry, and further tested using bioassays to confirm growth inhibition activity. We sequenced the genome of one actinobacterial isolate [48] to confirm this strains' phylogenetic identification, and identified a putative biosynthetic gene cluster for one of the characterized active compounds. Based on these results, we propose a mutualism between two species of ambrosia beetle and Actinobacteria, in which the bacterial symbiont produces cycloheximide to inhibit the growth of fungal competitors of the mutualistic cultivar fungus.…”

Section: Introductionmentioning

confidence: 99%

Cycloheximide-ProducingStreptomycesAssociated withXyleborinus saxeseniiandXyleborus affinisFungus-Farming Ambrosia Beetles

Grubbs

Surup

Biedermann

et al. 2019

Preprint

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25Symbiotic microbes help a myriad of insects acquire nutrients. Recent work suggests that insects 26 also frequently associate with actinobacterial symbionts that produce molecules to help defend 27 against parasites and predators. Here we explore a potential association between Actinobacteria 28 and two species of fungus-farming ambrosia beetles, Xyleborinus saxesenii and Xyleborus 29 affinis. We isolated and identified actinobacterial and fungal symbionts from laboratory reared 30 nests, and characterized small molecules produced by the putative actinobacterial symbionts. 31 One 16S rRNA phylotype of Streptomyces (XylebKG-1) was abundantly and consistently 32 isolated from the nests and adults of X. saxesenii and X. affinis nests. In addition to Raffaelea 33 sulphurea, the symbiont that X. saxesenii cultivates, we also repeatedly isolated a strain of 34 Nectria sp. that is an antagonist of this mutualism. Inhibition bioassays between S. griseus 35 XylebKG-1 and the fungal symbionts from X. saxesenii revealed strong inhibitory activity of the 36 actinobacterium towards the fungal antagonist Nectria sp. but not the fungal mutualist R. 37 sulphurea. Bioassay guided HPLC fractionation of S. griseus XylebKG-1 culture extracts, 38 followed by NMR and mass spectrometry identified cycloheximide as the compound responsible 39 for the observed growth inhibition. A biosynthetic gene cluster putatively encoding 40 cycloheximide was also identified in S. griseus XylebKG-1. The consistent isolation of a single 41 16S phylotype of Streptomyces from two species of ambrosia beetles, and our finding that a 42 representative isolate of this phylotype produces cycloheximide, which inhibits a parasite of the 43 system but not the cultivated fungus, suggests that these actinobacteria may play defensive roles 44 within these systems. 45[15-21]. Reliance on fungi by these insects exposes them to potential parasite pressure in the 69 form of pathogens or competitors of their symbionts. For example, the fungal mutualist of attine 70 ants is impacted by a specialized and potentially virulent fungal parasite [22, 23]. To help defend 71 the cultivar from this parasite the ants use actinobacterial symbionts that produce antibiotics [23-72 26]. A similar type of defensive symbiosis has been shown in the fungus-associated bark beetle 73 Dendroctonus frontalis [27], and has been further suggested in the Mediterranean Pine Engraver 74 bark beetle, Orthotomicus erosus [28], as well as fungus-growing termites [29]. Beyond 75 defending fungal mutualists in agricultural associations, Actinobacteria are well adapted for 76 insect dispersal (e.g. by desiccation-resistant, hydrophobic spores that stick to the surface of 77 insects [30]) and fulfill different defensive capacities in other insect systems. Within antennal 78 glands, Beewolves (Philanthus spp.) cultivate Actinobacteria that they transfer into brood cells 79 and onto developing cocoons in order to prevent infection by a wide range of pathogens [31]. 80 Actinobacteria and the antibio...

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“…HTCC2649, sequence accession AAMN00000000 [133] Microbacterium testaceum StLB037, sequence accession AP012052 [134] Mycobacterium bovis BCG, sequence accession later [135] Nocardioides sp. JS614, sequence accession CP000509, CP000508 [136] Saccharopolyspora spinosa NRRL 18395, sequence accession AEYC00000000 [137] Streptomyces griseoaurantiacus, sequence accession AEYX01000000 [138] Streptomyces griseus XyelbKG-1, sequence accession ADFC00000000 [139] Streptomyces sp. PP-C42, sequence accession AEWS01000000 [140] Verrucosispora maris AB-18-032, sequence accession CP002638, CP002639 [141] Phylum Chlamydiae Chlamydia pecorum E58, sequence accession CP002608 [142] Chlamydia psittaci 6BC, sequence accession CP002586 (chromosome), CP002587 (plasmid) [143] Chlamydia psittaci Cal10, sequence accession AEZD00000000 [143] Chlamydophila psittaci RD1, sequence accession FQ482149 (chromosome) FQ482150 (plasmid) [144] Standards in Genomic Sciences…”

Section: Phylum Tenericutesmentioning

confidence: 99%

Genome sequences published outside of Standards in Genomic Sciences, January – June 2011

Nelson

2011

Stand. Genomic Sci.

122

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Genome Sequence of Streptomyces griseus Strain XylebKG-1, an Ambrosia Beetle-Associated Actinomycete

Cited by 25 publications

References 19 publications

Abundance and dynamics of filamentous fungi in the complex ambrosia gardens of the primitively eusocial beetleXyleborinus saxeseniiRatzeburg (Coleoptera: Curculionidae, Scolytinae)

Abundance and dynamics of filamentous fungi in the complex ambrosia gardens of the primitively eusocial beetleXyleborinus saxeseniiRatzeburg (Coleoptera: Curculionidae, Scolytinae)

Cycloheximide-ProducingStreptomycesAssociated withXyleborinus saxeseniiandXyleborus affinisFungus-Farming Ambrosia Beetles

Genome sequences published outside of Standards in Genomic Sciences, January – June 2011

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