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Origin and Examination of a Leafhopper Facultative Endosymbiont

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Origin and Examination of a Leafhopper Facultative Endosymbiont Origin and Examination of a Leafhopper Facultative Endosymbiont The Harvard community has made this article openly available. Please share how this access benefits you. Your story matters Citation Degnan, Patrick H., Leonora S. Bittleston, Allison K. Hansen, Zakee L. Sabree, Nancy A. Moran, and Rodrigo P. P. Almeida. 2011. Origin and Examination of a Leafhopper Facultative Endosymbiont. Current Microbiology 62(5): 1565-1572. Published Version doi://10.1007/s00284-011-9893-5 Citable link http://nrs.harvard.edu/urn-3:HUL.InstRepos:11213355 Terms of Use This article was downloaded from Harvard University’s DASH repository, and is made available under the terms and conditions applicable to Other Posted Material, as set forth at http:// nrs.harvard.edu/urn-3:HUL.InstRepos:dash.current.terms-of- use#LAA Curr Microbiol (2011) 62:1565–1572 DOI 10.1007/s00284-011-9893-5 Origin and Examination of a Leafhopper Facultative Endosymbiont Patrick H. Degnan • Leonora S. Bittleston • Allison K. Hansen • Zakee L. Sabree • Nancy A. Moran • Rodrigo P. P. Almeida Received: 23 November 2010 / Accepted: 1 February 2011 / Published online: 19 February 2011 Ó The Author(s) 2011. This article is published with open access at Springerlink.com Abstract Eukaryotes engage in intimate interactions with 12% of the BEV genome. Nearly half of the gene fragments microbes that range in age and type of association. were similar to mobile DNA, including 15 distinct types of Although many conspicuous examples of ancient insect insertion sequences (IS). Analyses revealed that BEV not associates are studied (e.g., Buchnera aphidicola), fewer only shares virulence genes with plant pathogens, but also is examples of younger associations are known. Here, we closely related to the plant pathogenic genera Dickeya, further characterize a recently evolved bacterial endosym- Pectobacterium, and Brenneria. However, the slightly biont of the leafhopper Euscelidius variegatus (Hemiptera, reduced genome size, abundance of mobile DNA, fastidious Cicadellidae), called BEV. We found that BEV, continu- growth in culture, and efficient vertical transmission sug- ously maintained in E. variegatus hosts at UC Berkeley gest that symbiosis with E. variegatus has had a significant since 1984, is vertically transmitted with high fidelity. impact on genome evolution in BEV. Unlike many vertically transmitted, ancient endosymbioses, the BEV–E. variegatus association is not obligate for either partner, and BEV can be cultivated axenically. Sufficient Introduction BEV colonies were grown and harvested to estimate its genome size and provide a partial survey of the genome Bacterial interactions with insect hosts have pronounced sequence. The BEV chromosome is about 3.8 Mbp, and consequences for bacterial lifestyles and genome evolution. there is evidence for an extrachromosomal element roughly After millions of years of co-evolution, ancient insect en- 53 kb in size (e.g., prophage or plasmid). We sequenced dosymbionts have experienced irreversible changes in 438 kb of unique short-insert clones, representing about genome size and content, resulting in an inability to survive outside of hosts [24]. However, transitions from free-living to symbiotic lifestyles are likely ongoing in bacterial lin- P. H. Degnan and L. S. Bittleston contributed equally to this work. eages [1, 12, 18]. Recently evolved facultative symbionts Electronic supplementary material The online version of this provide the opportunity to examine the initial processes article (doi:10.1007/s00284-011-9893-5) contains supplementary that affected the genome evolution of long-term, obligate material, which is available to authorized users. endosymbionts. Such a symbiont was identified and culti- P. H. Degnan (&) Á A. K. Hansen Á Z. L. Sabree Á N. A. Moran vated from the leafhopper Euscelidius variegatus Department of Ecology and Evolutionary Biology, Yale (Hemiptera, Cicadellidae) [33], and its effects on hosts University, New Haven, CT, USA have been studied for over two decades. e-mail: [email protected] The bacterium of E. variegatus (BEV) is transovarially L. S. Bittleston transmitted [34], a factor that in some cases indicates long- Department of Organismic and Evolutionary Biology, Harvard term stability or mutualistic tendencies; however, BEV University, Cambridge, MA, USA reduces the fitness of its host and is highly pathogenic when injected into other leafhopper species [6, 33, 34]. R. P. P. Almeida Department of Environmental Science, Policy and Management, When tested in 1987, infected E. variegatus displayed University of California Berkeley, Berkeley, CA, USA reduced fecundity, longevity, and increased development 123 1566 P. H. Degnan et al.: Origin and Examination of a Leafhopper Facultative Endosymbiont time [34]; since then, the degree of pathogenicity may have visualized with ethidium bromide (EtBr) and several were declined, under laboratory conditions. BEV can be hori- randomly sequenced for confirmation. zontally acquired by naı¨ve hosts when feeding on plants in the company of infected individuals, but it does not move, Estimation of BEV Growth Rate replicate, or cause disease within plants [35]. Microscopy of E. variegatus indicates that BEV cells are present in the A triple-cloned isolate (re-plated using a single colony, hemolymph and invade the ovaries and midgut epithelium three times) was plated as a lawn on PB agar, collected and leading to tissue degeneration in the latter [5, 6]. BEV’s used to inoculate two replicate 1 ml liquid PB cultures. ability to penetrate into different host tissues and avoid the Two sets of ten culture tubes were then inoculated from insect immune system may be due in part to a tolerance for each of the replicates, wrapped in foil, and incubated at acidic conditions. Even at a pH of 5.2, BEV exhibited cell 28°C and shaken at 180 rpm. Culture tubes from each growth over a period of 24 h (Alexander Purcell, personal replicate were removed serially starting at day zero, plated communication). Unlike obligate endosymbionts of insects, and colony-forming units per milliliter (CFU/ml) were BEV is not essential for its hosts’ survival or reproduc- counted. tion [23]. Additionally, BEV remains one of the few endosymbionts that can be cultivated axenically [32]. Genome Size Determination Here, we evaluated the efficiency of BEV vertical transmission in E. variegatus and calculated its growth rate Briefly, BEV DNA was purified for pulsed-field gel elec- in culture. Sequencing endosymbiont genomes generally trophoresis (PFGE) by first scraping colonies from PB agar requires complex isolation and enrichment techniques to plates and spinning down the cells. Then, the pellet was acquire DNA for sequencing. However, we have taken resuspended in PBS, mixed with an equal volume of 1.5% advantage of the ability to grow BEV in culture to make a w/v pulsed-field gel agarose (BioRad) in TE (10 mM Tris preliminary survey of its genome size, content, and phy- pH 8.0, 1 mM EDTA pH 8.0) and solidified in plastic plug logenetic origins. molds. The plugs, containing intact cells, were then lysed, washed, and digested with the homing endonuclease I-CeuI (NEB). Plugs and appropriate size standards were sepa- Materials and Methods rated on a PFGE rig (BioRad) using 0.59 TBE buffer, 1% w/v pulsed-field agarose gels and run conditions listed in History of the BEV Colony the Supplemental Methods. Gels were visualized with EtBr and fragment sizes were estimated manually by measuring BEV was discovered by Alexander Purcell in laboratory fragment migration of the size standard and plotting it by colonies of the leafhopper E. variegatus in Pont-de-la- size on a semi-log plot. Maye, France and has been maintained at UC Berkeley since 1984 [33]. Unfortunately, original material (insect or BEV Genome Library Construction and Annotation bacterial) from 1984 is not available. Infected leafhoppers are reared on a mix of barley, rye, and wheat grasses that Total genomic DNA was extracted from a single triple- are changed every 1 to 2 weeks. For the following exper- cloned BEV isolate grown on PB agar using the DNeasy iments, BEV was axenically cultured from leafhoppers on Blood and Tissue Kit (Qiagen, Valencia, CA). This Difco purple broth (PB) with 1.5–2.0% agar, acidified to required two extractions to obtain a 20 lg pooled DNA pH 6.3 with 0.1 N HCl and incubated at 28°C in the dark sample (as determined by UV spectrophotometery). This [33]. sample was used to generate a blunt-end, short-insert pUC19 library according to published protocols [36] Quantifying Vertical Transmission Efficiency of BEV (Supplemental Methods). Transformants bearing plasmids were purified using a boiling mini prep protocol [36], Ten cages were prepared each containing four rye grass quantified, and Sanger sequenced with M13F primer on an plants and twenty BEV-infected E. variegatus adults. The ABI3730xl (Life Technologies). Individual BEV reads adults were allowed to oviposit for 7 days then removed were trimmed, dereplicated, and annotated following and frozen. After 5 days of maturation, 5–7 eggs per cage standard protocols [11]. Reads containing identical trans- were collected and surface sterilized. DNA was extracted posase gene fragments were manually clustered then from the eggs and screened with BEV specific 16S ribo- assembled into complete insertion sequences. Raw somal RNA (rRNA) PCR primers (see Supplemental sequence reads have been submitted to the GenBank Trace Methods). Amplicons were run on a 1% agarose gel and Archive (2292004866–2292005569).
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