Abstract
BackgroundThe carpenter ant Camponotus floridanus harbors obligate intracellular mutualistic bacteria (Blochmannia floridanus) in specialized cells, the bacteriocytes, intercalated in their midgut tissue. The diffuse distribution of bacteriocytes over the midgut tissue is in contrast to many other insects carrying endosymbionts in specialized tissues which are often connected to the midgut but form a distinct organ, the bacteriome. C. floridanus is a holometabolous insect which undergoes a complete metamorphosis. During pupal stages a complete restructuring of the inner organs including the digestive tract takes place. So far, nothing was known about maintenance of endosymbionts during this life stage of a holometabolous insect. It was shown previously that the number of Blochmannia increases strongly during metamorphosis. This implicates an important function of Blochmannia in this developmental phase during which the animals are metabolically very active but do not have access to external food resources. Previous experiments have shown a nutritional contribution of the bacteria to host metabolism by production of essential amino acids and urease-mediated nitrogen recycling. In adult hosts the symbiosis appears to degenerate with increasing age of the animals.ResultsWe investigated the distribution and dynamics of endosymbiotic bacteria and bacteriocytes at different stages during development of the animals from larva to imago by confocal laser scanning microscopy. The number of bacteriocytes in relation to symbiont-free midgut cells varied strongly over different developmental stages. Especially during metamorphosis the relative number of bacteria-filled bacteriocytes increased strongly when the larval midgut epithelium is shed. During this developmental stage the midgut itself became a huge symbiotic organ consisting almost exclusively of cells harboring bacteria. In fact, during this phase some bacteria were also found in midgut cells other than bacteriocytes indicating a cell-invasive capacity of Blochmannia. In adult animals the number of bacteriocytes generally decreased.ConclusionsDuring the life cycle of the animals the distribution of bacteriocytes and of Blochmannia endosymbionts is remarkably dynamic. Our data show how the endosymbiont is retained within the midgut tissue during metamorphosis thereby ensuring the maintenance of the intracellular endosymbiosis despite a massive reorganization of the midgut tissue. The transformation of the entire midgut into a symbiotic organ during pupal stages underscores the important role of Blochmannia for its host in particular during metamorphosis.
Highlights
The carpenter ant Camponotus floridanus harbors obligate intracellular mutualistic bacteria (Blochmannia floridanus) in specialized cells, the bacteriocytes, intercalated in their midgut tissue
Bacteriocyte distribution in larvae of C. floridanus The distribution of endosymbiont containing bacteriocytes within the host midgut tissue was investigated by fluorescence in-situ hybridization (FISH) and direct fluorescence labeling of bacteria and host cells over different developmental stages
In conclusion, the data presented here demonstrate that there is a permanent presence of bacteriocytes during pupal stages ensuring that the intracellular endosymbionts are not lost during the complex process of metamorphosis which involves a reconstruction of the inner organs of the insect including the digestive tract
Summary
The carpenter ant Camponotus floridanus harbors obligate intracellular mutualistic bacteria (Blochmannia floridanus) in specialized cells, the bacteriocytes, intercalated in their midgut tissue. Bacteriocyte endosymbiosis is a widespread phenomenon in insects with an estimated 15 to 20% of all insects harboring obligate intracellular endosymbionts [1] These socalled primary endosymbionts are harbored in specialized tissues, e.g. within the midgut tissue of carpenter ants, where they are intercalated between midgut cells [4,5]. Within the bacteriocyte the bacteria can either be surrounded by a host derived symbiosomal membrane, e.g. Buchnera in aphids [2,6], or they reside in the cytoplasm, e.g. Blochmannia in ants [5] These bacteria are confined to intracellular locations, for instance, Wigglesworthia, the primary endosymbiont of tsetse flies, can be found extracellularly in the milk gland lumen from where the bacteria can infect the developing brood [7]. Observations indicated that Blochmannia may have a cell invasive capacity, when the bacteria evade from bacteriocytes in the midgut tissue in order to infiltrate the oocytes guaranteeing the vertical transmission of the bacteria [9]
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