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Cultivation and Characterization of the Gut Symbionts of Honey Bees and Bumble Bees: Description of Snodgrassella Alvi Gen

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Cultivation and Characterization of the Gut Symbionts of Honey Bees and Bumble Bees: Description of Snodgrassella Alvi Gen International Journal of Systematic and Evolutionary Microbiology (2013), 63, 2008–2018 DOI 10.1099/ijs.0.044875-0 Cultivation and characterization of the gut symbionts of honey bees and bumble bees: description of Snodgrassella alvi gen. nov., sp. nov., a member of the family Neisseriaceae of the Betaproteobacteria, and Gilliamella apicola gen. nov., sp. nov., a member of Orbaceae fam. nov., Orbales ord. nov., a sister taxon to the order ‘Enterobacteriales’ of the Gammaproteobacteria Waldan K. Kwong and Nancy A. Moran Correspondence Department of Ecology and Evolutionary Biology, Yale University, 165 Prospect Street, New Haven, Waldan K. Kwong CT 06511, USA [email protected] Gut-associated bacteria were isolated in axenic culture from the honey bee Apis mellifera and the bumble bees Bombus bimaculatus and B. vagans and are here placed in the novel genera and species Snodgrassella alvi gen. nov., sp. nov. and Gilliamella apicola gen. nov., sp. nov. Two strains from A. mellifera were characterized and are proposed as the type strains of Snodgrassella alvi (type strain wkB2T 5NCIMB 14803T 5ATCC BAA-2449T 5NRRL B-59751T) and Gilliamella apicola (type strain wkB1T 5NCIMB 14804T 5ATCC BAA-2448T), representing, respectively, phylotypes referred to as ‘Betaproteobacteria’ and ‘Gammaproteobacteria-1’/ ‘Gamma-1’ in earlier publications. These strains grew optimally under microaerophilic conditions, and did not grow readily under a normal atmosphere. The predominant fatty acids in both strains were palmitic acid (C16 : 0) and cis-vaccenic acid (C18 : 1v7c and/or C18 : 1v6c), and both strains had ubiquinone-8 as their major respiratory quinone. The DNA G+C contents were 41.3 and 33.6 mol% for wkB2T and wkB1T, respectively. The Snodgrassella alvi strains from honey bees and bumble bees formed a novel clade within the family Neisseriaceae of the Betaproteobacteria, showing about 94 % 16S rRNA gene sequence identity to their closest relatives, species of Stenoxybacter, Alysiella and Kingella.TheGilliamella apicola strains showed the highest 16S rRNA gene sequence identity to Orbus hercynius CN3T (93.9 %) and several sequences from uncultured insect-associated bacteria. Phylogenetic reconstruction using conserved, single- copy amino acid sequences showed Gilliamella apicola as sister to the order ‘Enterobacteriales’ of the Gammaproteobacteria. Given its large sequence divergence from and basal position to the well-established order ‘Enterobacteriales’, we propose to place the clade encompassing Gilliamella apicola and O. hercynius in a new family and order, Orbaceae fam. nov. and Orbales ord. nov. The GenBank/EMBL/DDBJ accession numbers for the 16S rRNA gene Honey bees and bumble bees are generalist insect sequences of strains wkB2T, wkB12 and wkB29 are JQ746645– pollinators that play a key role in maintaining healthy JQ746651, while those of strains wkB1T, wkB11 and wkB30 are ecosystem function. In addition, the Western honey bee, JQ936674–JQ936676. Accession numbers for the ack gene Apis mellifera, is of great importance to human agriculture, sequences of strains wkB2T and wkB12 are JQ746652 and JQ746653, respectively. Accession numbers of protein-coding gene producing products such as honey and pollinating many of sequences of strains wkB1T, wkB11 and wkB30 determined in this the world’s crops. Despite substantial interest in bee health study are JQ894901–JQ894930, as detailed in Table S1. and disease, little is known about the normal microbial A supplementary table and two supplementary figures are available with flora in bees. Bacteria that live in close, symbiotic the online version of this paper. association with insects can perform beneficial functions 2008 044875 G 2013 IUMS Printed in Great Britain Cultivation of the gut symbionts of bees including nutrient synthesis, digestion and provision of by either a CO2 incubator set at 5 % CO2 or CO2Gen disease resistance (Dillon & Dillon, 2004; Koch & Schmid- Compact sachets (Oxoid) in airtight pouches, which Hempel, 2011b). Honey bees (Apis spp.) and bumble bees produced a 6 % CO2,15%O2 atmosphere. (Bombus spp.) have recently been found to possess a highly Colonies were visible after 2 days and were identified by specific gut microbial composition, suggesting they too sequencing of the 16S rRNA gene. DNA was extracted using may participate in an intimate host–microbe symbiosis the Qiagen DNeasy Blood & Tissue kit according to its (Martinson et al., 2011; Koch & Schmid-Hempel, 2011a). protocol for Gram-negative bacteria. PCR amplicons were The unique bee gut microbiota consists mainly of eight generated using the universal 16S primers 27F (59- bacterial phylotypes: two from the Alphaproteobacteria, two AGAGTTTGATCCTGGCTCAG-39) and 1492R (59-GGTT- from the Gammaproteobacteria, two from Lactobacillus, one ACCTTGTTACGACTT-39) with 35 cycles of amplification from Bifidobacterium and one from the Betaproteobacteria (95 uC for 20 s, 52 uC for 30 s and 72 uC for 40 s) after an (Martinson et al., 2011; Moran et al., 2012). Although there initial incubation for 10 min at 95 uC. Amplicons were has been a long history of culture-based studies of bee sequenced using the dideoxy chain-termination method microbes (Gilliam, 1997), the characteristic bacteria that with the Big Dye Terminator version 3.1 kit and subsequent make up most of the bee gut microbiota are mostly known capillary gel electrophoresis on an Applied Biosystems from 16S rRNA gene sequencing (Jeyaprakash et al., 2003; 3730xl DNA Genetic Analyzer (DNA Analysis Facility, Yale University). In order to determine the species identity of Babendreier et al., 2007; Martinson et al., 2011; Koch & wild-captured bumble bees, the COI gene was sequenced Schmid-Hempel, 2011a; Disayathanoowat et al., 2012; from bee tissue with primers LEP-F1 and LEP-R1, as Moran et al., 2012) and from a recent metagenomic survey described previously (Hebert et al., 2004), and compared (Engel et al., 2012). Some culturing of these bacteria has using BLAST against annotated sequences in GenBank. been reported (Olofsson & Va´squez, 2008; Yoshiyama & Kimura, 2009; Killer et al., 2009, 2010; Koch & Schmid- As part of a multigenome sequencing project, the genomes Hempel, 2011b; Engel et al., 2012), but most of these of strains wkB2T, wkB12, wkB29, wkB1T, wkB11 and wkB30 phylotypes remain undescribed. were sequenced using the Illumina platform from mate-pair libraries (data not shown). Sequence assembly of raw reads Here, we report the isolation and characterization of members into contigs was performed with Velvet 1.1.06 (Zerbino & of the ‘Betaproteobacteria’ and ‘Gammaproteobacteria-1’/ Birney, 2008). Accession numbers of sequences from this ‘Gamma-1’ groups (Babendreier et al., 2007; Martinson et al., study used to produce Fig. 5 are listed in Table S1 (available 2011) from A. mellifera and Bombus species, and propose in IJSEM Online). All phylogenetic analysis was done with novel genera and species, Snodgrassella alvi gen. nov., sp. nov. the MEGA 5 software package (Tamura et al., 2011). and Gilliamella apicola gen. nov., sp. nov., respectively, in which to place members of these groups. These names are For transmission electron microscopy imaging, 2-day-old consistent with those proposed by Martinson et al. (2012), cultures from blood-agar plates were harvested in trypticase ‘Candidatus Snodgrassella alvi’ and ‘Candidatus Gilliamella soy broth (TSB), pelleted and fixed with 4 % glutaraldehyde in 0.1 M Sorensen’s phosphate buffer (PB) (162 mM apicola’. Strains wkB2T and wkB1T from A. mellifera are Na HPO , 32 mM NaH PO ), pH 7.4, for 1 h. Cells were proposed as the respective type strains of Snodgrassella alvi 2 4 2 4 then washed with Sorensen’s PB and fixed with 1 % osmium and Gilliamella apicola. We also provide evidence to support tetroxide in distilled water for 1 h. Following rinsing with the position of the Gilliamella apicola clade as sister to the distilled water, the samples were dehydrated with successive family Enterobacteriaceae/order ‘Enterobacteriales’. Given the 70, 80, 90 and 100 % ethanol washes. Samples were then genetic and phenotypic similarity of Gilliamella apicola to T washed with propylene oxide before incubating in Embed- Orbus hercynius CN3 (Volkmann et al.,2010),weproposea 812/propylene oxide mixture (1 : 1) for 1 h and then novel family and order in which to place this group, Orbaceae overnight in 2 : 1 Embed-812/propylene oxide mixture. fam. nov. and Orbales ord. nov. Finally, samples were immersed in pure Embed-812 and cured under vacuum overnight at 50 uC. Sections of 60– Methods 100 nm thickness were cut and stained with uranyl acetate Bacterial strains were isolated from the gut of the Western and lead citrate, and these were viewed with a Zeiss EM-900 honey bee, A. mellifera, and the bumble bees Bombus transmission electron microscope. bimaculatus and Bombus vagans. Adult worker bees, A. Biochemical and metabolic tests were conducted to character- mellifera from lab-raised hives and Bombus species wild ize the isolates further. Catalase activity was tested by adding foragers, were captured in West Haven, CT, USA, in May cells directly to 3 % H2O2 andobservedforthegenerationof and June 2011. Bees were immobilized by chilling at 4 uC gas. Presence of cytochrome c oxidase was determined by before the guts were dissected out and homogenized in smearing cells onto filter paper wetted with Gordon–McLeod 10 mM MgSO4 by bead beating. The homogenates were reagent (Sigma). Sulfide-indole-motility (SIM) medium plated on HIA (heart infusion agar; Difco BD) and blood (Hardy Diagnostics) was used to test for H2Sproduction agar (tryptic soy agar supplemented with 5 % sheep’s and motility. The API 20NE kit (bioMe´rieux) was used to blood; Hardy Diagnostics) and incubated at 37 uCina determine activities of nitrate and nitrite reductases, arginine CO2-enriched atmosphere. The atmosphere was provided dihydrolase, urease, b-glucosidase (aesculinase), gelatinase http://ijs.sgmjournals.org 2009 W. K. Kwong and N. A. Moran and b-galactosidase (substrate PNPG) and for glucose Characterization of Snodgrassella alvi gen. nov., fermentation and indole production according to the sp. nov.
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