Endosymbiotic microorganisms of aphids (Hemiptera: Sternorrhyncha: Aphidoidea): Ultrastructure, distribution and transovarial transmission

Abstract

Abstract. The ultrastructure, distribution and transovarial transmission of endosymbiotic bacteria in representatives of six aphid families: Eriosomatidae (Pemphigus spyrothecae, Prociphilus fraxini), Anoeciidae [Anoecia (Anoecia) corni], Drepanosiphidae [Mindarus abietinus, Sipha (Rungsia) maydis, Clethrobius comes, Myzocallis (Lineomyzocallis) walshii], Thelaxidae (Thelaxes dryophila), Aphididae (Delphiniobium junackianum, Aphis viburni, Cavariella theobaldi, Macrosiphoniella tanacetaria) and Lachnidae (Schizolachnus pineti, Eulachnus rileyi) were studied at the ultrastructural level. The ovaries of aphids are accompanied by large organs termed bacteriomes that consist of giant cells termed bacteriocytes. The bacteriocyte cytoplasm is tightly packed with endosymbiotic bacteria. Ultrastructural observations have shown that the bacteria Buchnera aphidicola (primary symbiont of aphids) present in various species are characterized by significant differences in both size and organization of their cytoplasm. In the aphids, Prociphilus fraxini, Sipha (Rungsia) maydis, Thelaxes dryophila, Aphis viburni, Cavariella theobaldi, Macrosiphoniella tanacetaria, Eulachnus rileyi and Schizolachnus pineti, in addition to Buchnera aphidicola, secondary endosymbionts are also present. The bacteriocytes containing secondary endosymbionts are less numerous than those with Buchnera. In Eulachnus rileyi (Lachnidae), in addition to primary and secondary endosymbionts, there is a third type of microorganism. In all species examined both the primary and secondary endosymbionts are transovarially transmitted from mother to offspring.

Happens in the best of subfamilies: establishment and repeated replacements of co‐obligate secondary endosymbionts within Lachninae aphids

“…One crucial question within the field is how do these associations evolve. This fact, in combination with previously published microscopic (Buchner, 1953;Fukatsu and Ishikawa, 1998;Lamelas et al, 2008;Pyka-Fo sciak and Szklarzewicz, 2008;Michalik et al, 2014) . In the Lachninae subfamily of aphids, it has previously been proposed that an ancient loss of the riboflavin biosynthetic capability by Buchnera promoted the settlement of a co-obligate secondary endosymbiont (putatively S. symbiotica) in the LLCA (Manzano-Mar ın and Latorre, 2014; Manzano-Mar ın et al, 2016).…”

“…This has been evidenced through phylogenetic reconstructions using Buchnera DNA or amino acid sequences, which parallel their aphid hosts' evolutionary relationships (Munson et al, 1991;Jousselin et al, 2009;Liu et al, 2013). These secondary symbionts have a very different tissue tropism than Buchnera, as they can be present in separate bacteriocytes (called secondary bacteriocytes), coinfecting the primary endosymbiont's bacteriocytes, located in sheath cells (at the periphery of the bacteriome and found closely associated to bacteriocytes) and/or free in the haemocoel (Fukatsu et al, 2000;Sandstr€ om et al, 2001;Moran et al, 2005;Sakurai et al, 2005;Michalik et al, 2014). Contrary to obligate symbionts, facultative ones are not required for the correct development, reproduction and survival of their host.…”

“…Besides Buchnera, aphids can also harbour secondary endosymbionts (in addition to the primary symbiont), these being of facultative or obligate nature in some lineages. In this respect, the subfamily Lachninae Herrich-Schaeffer, 1854 of aphids is peculiar, in that all members analysed thus far by microscopy techniques have been found to house secondary endosymbionts (Buchner, 1953;Fukatsu and Ishikawa, 1998;Lamelas et al, 2008;Pyka-Fo sciak and Szklarzewicz, 2008;Michalik et al, 2014). Still, they can provide a benefit under certain environmental or ecological conditions (conditional mutualism) (reviewed in Oliver et al, 2010Oliver et al, , 2014.…”

Symbiotic microorganisms of the leafhopper Deltocephalus pulicaris (Fallén, 1806) (Insecta, Hemiptera, Cicadellidae: Deltocephalinae): molecular characterization, ultrastructure and transovarial transmission

“…Earlier histological analyses (MÜLLER 1962, BUCHNER 1965, as well as more recent ultrastructural ones, have shown that hemipterans developed various means of transmitting symbionts from one generation to the next (CHENG & HOU 2001, SZKLARZEWICZ & MOSKAL 2001, SZKLARZEWICZ et al 2006, SACCHI et al 2008, MICHALIK et al 2009, 2014a, 2014b, KUECHLER et al 2010, MATSUURA et al 2012, SWIATONIOWSKA et al 2013. Symbionts may infect larval ovaries containing undifferentiated germ cells or ovaries of adult females containing vitellogenic or choriogenic oocytes.…”

Symbiosis in the green leafhopper, Cicadella viridis (Hemiptera, Cicadellidae). Association in statu nascendi?

“…Both the histological (Müller, 1962;Buchner, 1965) and ultrastructural observations (Cheung and Purcell, 1999;Szklarzewicz and Moskal, 2001;Szklarzewicz et al, 2006Szklarzewicz et al, , 2013Sacchi et al, 2008;Michalik et al, 2009Michalik et al, , 2013Michalik et al, , 2014Kuechler et al, 2010Kuechler et al, , 2012Matsuura et al, 2012;Swiatoniowska et al, 2013) have revealed that hemipterans have developed different modes of transovarial transmission of bacteriocytes endosymbionts. These microorganisms may infest larval ovaries containing undifferentiated germ cells (¼cystocytes) or ovaries of adult females (in most hemipterans).…”