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Resedae (Heteroptera: Lygaeidae, Ischnorhynchinae) Stefan Martin Kuchler,¨ Konrad Dettner & Siegfried Kehl

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Resedae (Heteroptera: Lygaeidae, Ischnorhynchinae) Stefan Martin Kuchler,¨ Konrad Dettner & Siegfried Kehl RESEARCH ARTICLE Molecular characterization and localization of the obligate endosymbiotic bacterium in the birch catkin bug Kleidocerys resedae (Heteroptera: Lygaeidae, Ischnorhynchinae) Stefan Martin Kuchler,¨ Konrad Dettner & Siegfried Kehl Department of Animal Ecology II, University of Bayreuth, Bayreuth, Germany Correspondence: Stefan Martin Kuchler, ¨ Abstract Department of Animal Ecology II, University of Bayreuth, Universitatsstraße¨ 30, 95440 In contrast to specific bacterial symbionts of many stinkbugs, which are harboured Bayreuth, Germany. Tel.: 149 921 552733; extracellularly in the lumina of midgut sacs or tubular outgrowths, the obligate fax: 149 921 552743; e-mail: endosymbiont of birch catkin bug Kleidocerys resedae (Heteroptera: Lygaeidae) [email protected] resides in a red-coloured, raspberry-shaped mycetome, localized abdominally, close to the midgut section. Phylogenetic analysis, based on the 16S rRNA gene and Received 21 December 2009; revised 23 March the groEL (chaperonin) gene, showed that the bacteria belong to the g-subdivision 2010; accepted 8 April 2010. of the Proteobacteria and revealed a phylogenetic relationship with bacterial Final version published online 25 May 2010. endosymbionts of Wigglesworthia glossinidia, the primary symbiont of tse-tse fly Glossina brevipalpis. Furthermore, RFLP analysis and sequencing revealed that DOI:10.1111/j.1574-6941.2010.00890.x K. resedae was also infected by Alphaproteobacteria of the genera Wolbachia and Editor: Michael Wagner Rickettsia. The distribution and transmission of Kleidocerys endosymbiont in adults and all nymph stages were studied using FISH. The detection of symbionts Keywords at the anterior poles of developing eggs indicated that endosymbionts are Gammaproteobacteria; Kleidocerys; Lygaeidae; transmitted vertically to offspring. Ultrastructural examinations by electron groEL; electron microscopy. microscopy revealed the packed accommodation of rod-shaped bacteria in the cytoplasm of mycetocytes. A new genus and species name, ‘Candidatus Kleidoceria schneideri’, is proposed for this newly characterized clade of symbiotic bacteria. (Buchner, 1965). On the other hand, facultative symbiotic Introduction bacteria (secondary symbionts or S-symbionts) are errati- Symbiotic bacteria have diverse ecological and evolutionary cally distributed and are not essential for host survival and effects on hosts, influencing aspects of ecological interac- reproduction. Nevertheless, facultative mutualists also exert tions from nutrition to defence and affecting reproductive fitness benefits, such as protection against natural enemies, systems, with consequences for population structure, repro- and resistance to pathogenic fungi, heat and other mortality ductive isolation and speciation (Buchner, 1965; Moran factors (Kellner, 2002; Russell & Moran, 2006; Kaltenpoth & et al., 2008). In particular, the most intimate mutualistic Strohm, 2007; Scott et al., 2008), allowing their carriers to associations are found in obligate insect symbionts (called live longer and reproduce more offspring. In contrast, primary symbionts or P-symbionts), which are required for facultative symbionts such as Rickettsia or Wolbachia can successful host development and reproduction of their also appear as reproductive manipulators that cause repro- hosts, exemplified by provisioning of essential nutrients in ductive aberrations such as cytoplasmatic incompatibility, aphids (Douglas, 1998, 2006), tse-tse flies (Akman et al., male-killing, feminization of genetic males and partheno- 2002) and carpenter ants (Sauer et al., 2000). In general, they genesis. The maternally inherited manipulators increase the are inherited, usually maternally, and lack a replicative or a host reproduction through daughters, often at the expense MICROBIOLOGY ECOLOGY MICROBIOLOGY dormant phase outside their hosts. Typically, primary sym- of reproduction through sons, and the host fitness in general bionts are restricted to special cells, called mycetocytes or (Stouthamer et al., 1999; Perlman et al., 2006). bacteriocytes, which are summarized in a compact symbio- Members of the Hemiptera, such as cicadas, aphids, tic organ – the mycetome or the bacteriome, respectively mealybugs and whiteflies, exhibit a strong phytophageous c 2010 Federation of European Microbiological Societies FEMS Microbiol Ecol 73 (2010) 408–418 Published by Blackwell Publishing Ltd. All rights reserved Primary endosymbiont of birch catkin bug Kleidocerys resedae 409 living, by sucking extremely unbalanced plant sap. Feeders endocellular symbionts of other insects, show remarkable of plant sap are well provided with carbohydrates available evolutionary patterns, including AT-biased nucleotide com- in the form of sucrose, but are not adequately supplied with position, accelerated molecular evolution and reduced gen- lipids, proteins, amino acids or vitamins. These shortfalls ome size (Hosokawa et al., 2006; Kikuchi et al., 2009). The will be compensated by the metabolic and biosynthetic important roles of these specific symbionts are especially capabilities of the primary symbionts of hemipteran insects, apparent in aposymbiotic nymphs of several heteropterans, best known in aphids, where the endosymbiont Buchnera where the absence of symbionts results in retarded growth aphidicola provides the host with essential amino acids and and/or nymphal mortality (Muller,¨ 1956; Abe et al., 1995; some vitamins (Douglas, 1998, 2003, 2006; Akman Gund¨ uz¨ Fukatsu & Hosokawa, 2002; Kikuchi et al., 2009). & Douglas, 2009). In the present study, we report the first molecular In addition to the ‘homopteran’ insects, most members of description of the endosymbiotic bacteria in the birch catkin Heteroptera, which feed on restricted diets – such as blood- bug Kleidocerys resedae (Heteroptera: Lygaeidae). Kleidocerys sucking bed bugs (Cimicidae), assassin bugs (Reduviidae)or resedae live on birch and alder trees (Betula spp. and Alnus plant-sapping bugs in different taxonomic groups – are spp.), feeding and breeding on the seed catkins (Wachmann dependent on a wide variety of symbiotic bacterial associa- et al., 2007) and are sometimes considered a ‘nuisance pest’ tions (Buchner, 1965; Dasch et al., 1984; Kikuchi et al., species because they invade homes in the autumn in large 2008). Both symbionts in the midgut epithelium and numbers (Sweet, 2000). As described in early histological abdominal mycetomes have been described for different studies, K. resedae exhibit a red-coloured, raspberry-shaped heteropteran bug species (Schneider, 1940; Chang & Mus- mycetome that overlies the midgut and runs in the long- grave, 1970; Dasch et al., 1984). itudinal direction of the body (Schneider, 1940). The grape- However, in many stinkbugs, specific bacterial symbionts shaped accumulation of mycetocytes, which are completely are harboured extracellularly in the lumina of midgut sacs or filled with Gammaproteobacteria, could be detected in all tubular outgrowths (Glasgow, 1914; Rosenkranz, 1939; larval stages and adults. Phylogenetic analysis inferred by Kikuchi & Fukatsu, 2008). These sac-like appendages of the 16S rRNA gene and particularly the groEL gene (chapero- posterior end of the midgut are called caeca or crypts and nin) revealed the phylogenetic position of the endosymbiont vary in number and arrangement in different taxonomic in the existing phylogenetic system of heritable endosym- groups. In most plant-sucking stinkbugs, the lumen of the bionts of insects. FISH was used to investigate bacterial midgut crypts is connected to the midgut main tract. distribution and vertical transmission. The morphological However, a complete separation of the lumen crypts from characteristics of the Gammaproteobacteria were analysed by the gut lumen has also been reported (Dasch et al., 1984; electron microscopic observations. Kikuchi et al., 2009). As a consequence of their extracellular associations in the gut cavity, the vertical transmission mechanisms of sym- Materials and methods bionts in heteropteran insects are more multifaceted than the transovarial mechanisms typical of intracellular symbio- Samples sis (Fukatsu & Nikoh, 2000; Braendle et al., 2003; Kikuchi Adults and larval stages of K. resedae were collected by heavy et al., 2007). Besides the direct superficial bacterial contam- shaking of birch branches (Betula spp.) on the university ination of egg surfaces (egg smearing; Pentatomidae, campus of Bayreuth in 2008 and 2009. Bugs were brought to Acanthosomatidae) (Rosenkranz, 1939; Abe et al., 1995), the laboratory alive and were embedded for histology/FISH two other impressive forms of transmission have been or dissected for bacteria characterization. reported: probing of parental bacteria-containing excrement (coprophagy; Cydnidae, Coreidae, Reduviidae) (Huber- Schneider, 1957; Schorr, 1957; Dasch et al., 1984; Beard Histology et al., 2002) and deposition of bacteria-containing capsules with eggs (capsule transmission; Plataspidae) (Schneider, Before all the bugs were fixed in 4% paraformaldehyde 1940; Muller,¨ 1956; Fukatsu & Hosokawa, 2002; Hosokawa overnight, the hemelytra were carefully removed. The fixed et al., 2005). Although such extracellular associations appear bugs were washed in 1 Â phosphate-buffered saline and 96% to be evolutionarily more casual than the endocellular ethanol (1 : 1), dehydrated serially in ethanol (70%, 90%, symbiosis, strict phylogenetic relationships of the gut sym- 2 Â 100%) and embedded in UnicrylTM (Plano GmbH, biont, except
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