Frischella perrara gen. nov., sp. nov., a gammaproteobacterium isolated from the gut of the honeybee, Apis mellifera

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dHere, we report the genome of one gammaproteobacterial member of the gut microbiota, for which we propose the name "Candidatus Schmidhempelia bombi," that was inadvertently sequenced alongside the genome of its host, the bumble bee, Bombus impatiens. This symbiont is a member of the recently described bacterial order Orbales, which has been collected from the guts of diverse insect species; however, "Ca. Schmidhempelia" has been identified exclusively with bumble bees. Metabolic reconstruction reveals that "Ca. Schmidhempelia" lacks many genes for a functioning NADH dehydrogenase I, all genes for the highoxygen cytochrome o, and most genes in the tricarboxylic acid (TCA) cycle. "Ca. Schmidhempelia" has retained NADH dehydrogenase II, the low-oxygen specific cytochrome bd, anaerobic nitrate respiration, mixed-acid fermentation pathways, and citrate fermentation, which may be important for survival in low-oxygen or anaerobic environments found in the bee hindgut. Additionally, a type 6 secretion system, a Flp pilus, and many antibiotic/multidrug transporters suggest complex interactions with its host and other gut commensals or pathogens. This genome has signatures of reduction (2.0 megabase pairs) and rearrangement, as previously observed for genomes of host-associated bacteria. A survey of wild and laboratory B. impatiens revealed that "Ca. Schmidhempelia" is present in 90% of individuals and, therefore, may provide benefits to its host.

Section: Resultsmentioning

confidence: 99%

Genomic Features of a Bumble Bee Symbiont Reflect Its Host Environment

Martinson

Magoč

Koch

et al. 2014

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“…This bacterium is less abundant than the other two species, with fewer bacteria present in the gut of individual bees, and in some cases, the bacterium is not present at all (5, 9, 12). Interestingly, all three bacteria have so far only been found associated with social bees and form deep-branching phylogenetic lineages exclusive of bacteria sampled from other environments (7,8,13), supporting longstanding symbiotic associations with their host and among each other.Bacterial symbionts frequently mediate interactions by using secondary metabolites, such as nonribosomal peptides and polyketides. These natural small molecules harbor a variety of activities, serving as mutualistic factors (14) Citation Engel P, Vizcaino MI, Crawford JM.…”

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confidence: 99%

“…In the anterior part of the honey bee hindgut, two gammaproteobacteria, Gilliamella apicola and Frischella perrara, and one betaproteobacterium, Snodgrassella alvi, are the dominant members of this gut community (7)(8)(9). Comparative genomics and functional analyses have recently revealed that S. alvi and G. apicola harbor complementary metabolic pathways, contain diverse sets of genes for symbiotic interactions, and exhibit host-specific colonization patterns (10,11).…”

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confidence: 99%

Gut Symbionts from Distinct Hosts Exhibit Genotoxic Activity via Divergent Colibactin Biosynthesis Pathways

Engel

Vizcaino

Crawford

2015

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e Secondary metabolites produced by nonribosomal peptide synthetase (NRPS) or polyketide synthase (PKS) pathways are chemical mediators of microbial interactions in diverse environments. However, little is known about their distribution, evolution, and functional roles in bacterial symbionts associated with animals. A prominent example is colibactin, a largely unknown family of secondary metabolites produced by Escherichia coli via a hybrid NRPS-PKS biosynthetic pathway that inflicts DNA damage upon eukaryotic cells and contributes to colorectal cancer and tumor formation in the mammalian gut. Thus far, homologs of this pathway have only been found in closely related Enterobacteriaceae, while a divergent variant of this gene cluster was recently discovered in a marine alphaproteobacterial Pseudovibrio strain. Herein, we sequenced the genome of Frischella perrara PEB0191, a bacterial gut symbiont of honey bees and identified a homologous colibactin biosynthetic pathway related to those found in Enterobacteriaceae. We show that the colibactin genomic island (GI) has conserved gene synteny and biosynthetic module architecture across F. perrara, Enterobacteriaceae, and the Pseudovibrio strain. Comparative metabolomics analyses of F. perrara and E. coli further reveal that these two bacteria produce related colibactin pathway-dependent metabolites. Finally, we demonstrate that F. perrara, like E. coli, causes DNA damage in eukaryotic cells in vitro in a colibactin pathway-dependent manner. Together, these results support that divergent variants of the colibactin biosynthetic pathway are widely distributed among bacterial symbionts, producing related secondary metabolites and likely endowing its producer with functional capabilities important for diverse symbiotic associations. C haracteristic bacterial communities colonize the digestive tracts of almost all animals and influence the health and disease of their hosts (1-4). These communities are typically dominated by specialist bacteria, which are adapted to live in the gut of their host and have evolved specific functions for symbiotic interactions. The honey bee, Apis mellifera, harbors such a characteristic gut microbiota (5). Its simple composition of only eight bacterial species makes the honey bee gut microbiota an ideal model to study the ecology and evolution of gut bacteria and to understand mutualistic, commensal, and parasitic relationships (6). Furthermore, honey bees are important pollinators for agriculture and almost all terrestrial ecosystems. Thus, it is essential to characterize the genomic capabilities of these symbiotic bacteria so as to better understand their impact on the health of their host.In the anterior part of the honey bee hindgut, two gammaproteobacteria, Gilliamella apicola and Frischella perrara, and one betaproteobacterium, Snodgrassella alvi, are the dominant members of this gut community (7-9). Comparative genomics and functional analyses have recently revealed that S. alvi and G. apicola harbor complementary metabolic pathways, co...

“…These three species have been axenically cultured and characterized biochemically and morphologically (15,16). The core microbiota also includes three species of Alphaproteobacteria ("Alpha-1," "Alpha-2.1," and "Alpha-2.2" [7]) and three Gram-positive species ("Bifido," corresponding to Bifidobacterium asteroides [17], and "Firm-4" and "Firm-5" [both Firmicutes: Lactobacillaceae]) (7).…”

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confidence: 99%

Routes of Acquisition of the Gut Microbiota of the Honey Bee Apis mellifera

Powell

Martinson

Urban‐Mead

et al. 2014

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431

491

bStudies of newly emerged Apis mellifera worker bees have demonstrated that their guts are colonized by a consistent core microbiota within several days of eclosure. We conducted experiments aimed at illuminating the transmission routes and spatiotemporal colonization dynamics of this microbiota. Experimental groups of newly emerged workers were maintained in cup cages and exposed to different potential transmission sources. Colonization patterns were evaluated using quantitative real-time PCR (qPCR) to assess community sizes and using deep sequencing of 16S rRNA gene amplicons to assess community composition. In addition, we monitored the establishment of the ileum and rectum communities within workers sampled over time from natural hive conditions. The study verified that workers initially lack gut bacteria and gain large characteristic communities in the ileum and rectum within 4 to 6 days within hives. Typical communities, resembling those of workers within hives, were established in the presence of nurse workers or nurse worker fecal material, and atypical communities of noncore or highly skewed compositions were established when workers were exposed only to oral trophallaxis or hive components (comb, honey, bee bread). The core species of Gram-negative bacteria, Snodgrassella alvi, Gilliamella apicola, and Frischella perrara, were dependent on the presence of nurses or hindgut material, whereas some Gram-positive species were more often transferred through exposure to hive components. These results indicate aspects of the colony life cycle and behavior that are key to the propagation of the characteristic honey bee gut microbiota.