Characterization of an Obligate Intracellular Bacterium in the Midgut Epithelium of the Bulrush Bug Chilacis typhae (Heteroptera, Lygaeidae, Artheneinae)

Abstract

Many members of the suborder Heteroptera have symbiotic bacteria, which are usually found extracellularly in specific sacs or tubular outgrowths of the midgut or intracellularly in mycetomes. In this study, we describe the second molecular characterization of a symbiotic bacterium in a monophagous, seed-sucking stink bug of the family Lygaeidae (sensu stricto). Chilacis typhae possesses at the end of the first section of the midgut a structure which is composed of circularly arranged, strongly enlarged midgut epithelial cells. It is filled with an intracellular endosymbiont. This "mycetocytic belt" might represent an evolutionarily intermediate stage of the usual symbiotic structures found in stink bugs. Phylogenetic analysis based on the 16S rRNA and the groEL genes showed that the bacterium belongs to the Gammaproteobacteria, and it revealed a phylogenetic relationship with a secondary bacterial endosymbiont of Cimex lectularius and free-living plant pathogens such as Pectobacterium and Dickeya. The distribution and ultrastructure of the rod-shaped Chilacis endosymbiont were studied in adults and nymph stages using fluorescence in situ hybridization (FISH) and electron microscopy. The detection of symbionts at the anterior poles of developing eggs indicates that endosymbionts are transmitted vertically. A new genus and species name, "Candidatus Rohrkolberia cinguli," is proposed for this newly characterized clade of symbiotic bacteria.

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

“…Buchner, 1965;Szklarzewicz & Moskal, 2001;Szklarzewicz et al, 2006Szklarzewicz et al, , 2010Szklarzewicz et al, , 2013Sacchi et al, 2008;Kuechler et al, 2012Kuechler et al, , 2013Swiatoniowska et al, 2013 for further details). Both the histological studies of Buchner (1965Buchner ( , 1966Buchner ( , 1967) and more recent ultrastructural studies (Cheng & Hou, 2001;Szklarzewicz & Moskal, 2001;Szklarzewicz et al, 2006Szklarzewicz et al, , 2010Szklarzewicz et al, , 2013Sacchi et al, 2008;Kuechler et al, 2011Kuechler et al, , 2012Koga et al, 2012;Matsuura et al, 2012;Swiatoniowska et al, 2013) have revealed that the latter transmission of endosymbionts (termed transovarial transmission) may differ even in closely related groups of hemipterans. The endosymbiotic microorganisms may invade young germ cells termed cystocytes (i.e.…”

“…Extensive, histological investigations by Buchner (1965) and more recent ultrastructural studies (Cheng & Hou, 2001;Szklarzewicz & Moskal, 2001;Szklarzewicz et al, 2006Szklarzewicz et al, , 2010Szklarzewicz et al, , 2013Sacchi et al, 2008;Kuechler et al, 2010Kuechler et al, , 2011Matsuura et al, 2012;Swiatoniowska et al, 2013) have shown that during hemipteran evolution various modes of inheritance of endosymbiotic microorganisms by subsequent generations have developed. The extracellular gut bacteria that are typical of most the heteropterans so far examined (i.e.…”

Diversity of Symbiotic Organs and Bacterial Endosymbionts of Lygaeoid Bugs of the Families Blissidae and Lygaeidae (Hemiptera: Heteroptera: Lygaeoidea)

“…Schneideria nysicola" but is phylogenetically close to "Ca. Rohrkolberia cinguli," the endosymbiont of Chilacis typhae (Artheneidae), which is harbored in enlarged epithelial cells of the midgut (28).…”

“…and Nysius spp. : a "bacteriocytic belt" exists at the anterior end of the midgut, which consists of circularly arranged, strongly enlarged midgut epithelial cells whose cytoplasm is full of a specific endosymbiont belonging to the Gammaproteobacteria (28). In all these cases, the endosymbionts are vertically transmitted via transovarial passages, which is typical of intracellular symbiotic associations (35).…”

“…Recently, several bacteriome-associated symbiotic systems of lygaeoid bugs were analyzed using molecular methods (27,28,32). In Kleidocerys resedae and Kleidocerys ericae (Lygaeoidea: Lygaeidae: Ischnorhynchinae), their endosymbiont, "Candidatus Kleidoceria schneideri" (Gammaproteobacteria), is harbored in a single red, raspberry-shaped bacteriome, which is closely associated with but not connected to the midgut (27).…”