Transcriptome analysis of the aphid bacteriocyte, the symbiotic host cell that harbors an endocellular mutualistic bacterium, Buchnera

Abstract

Aphids possess bacteriocytes, cells specifically differentiated to harbor obligatory mutualistic bacteria of the genus Buchnera, which have lost many genes that are essential for common bacterial functions. To understand the host's role in maintaining the symbiotic relationship, bacteriocytes were isolated from the pea aphid, Acyrthosiphon pisum, and the host transcriptome was investigated by using EST analysis and real-time quantitative RT-PCR. A number of genes were highly expressed specifically in the bacteriocyte, including (i) genes for amino acid metabolism, including those for biosynthesis of amino acids that Buchnera cannot produce, and those for utilization of amino acids that Buchnera can synthesize; (ii) genes related to transport, including genes for mitochondrial transporters and a gene encoding Rab, a G protein that regulates vesicular transport; and (iii) genes for putative lysozymes that degrade bacterial cell walls. Significant up-regulation of i clearly indicated that the bacteriocyte is involved in the exchange of amino acids between the host aphid and Buchnera, the key metabolic process in the symbiotic system. Conspicuously high expression of ii and iii shed light on previously unknown aspects of the host-Buchnera interactions in the symbiotic system.EST ͉ quantitative RT-PCR

Aphid genome expression reveals host–symbiont cooperation in the production of amino acids

“…2 and Table 1). Up-regulation of GS in bacteriocytes verifies previous findings based on limited numbers of ESTs and on quantitative PCR (14). Glutamine can contribute amino groups during synthesis of arginine and histidine.…”

“…GS was found to be highly expressed in bacteriocytes in our study as well as in a previous study (14), but this finding could reflect a role in detoxification of ammonia waste rather than a substantial role in supplementing the amino acid budget. Our results also show elevated expression of GltS, which was not previously detected in bacteriocyte ESTs.…”

“…Potentially, aphids themselves assimilate ammonia into amino acids, a possibility that is supported by the finding that GS, which produces glutamine from ammonia, is highly expressed in bacteriocytes (14). Glutamine has limited potential as a source of amino groups for production of other amino acids, but, together with glutamate synthase (GltS), it provides a shuttle for incorporating ammonia into most amino acids through glutamate.…”

“…This widespread presence in insects and other animals makes it unclear whether their presence in the aphid genome indicates a specific role in the amino acid production capacities of bacteriocytes (8). In a study based on a limited number of expressed sequence tags (ESTs) from A. pisum bacteriocytes (14), transcripts were retrieved from only two of these complementary aphid genes (encoding enzymes 1.14.16.1 and 4.4.1.1 in the methionine and tyrosine pathways, respectively).…”

A novel intracellular mutualistic bacterium in the invasive antCardiocondyla obscurior

“…Nutrient-providing symbionts are commonly found in hosts with restricted diets, for example, aphids feeding on phloem sap (Baumann, 2005), blood-feeding diptera (Wang et al, 2013) or grain weevils (Heddi et al, 1999). Symbionts can provide essential amino acids, vitamins or help in nitrogen recycling (Nakabachi et al, 2005;Feldhaar et al, 2007;Michalkova et al, 2014;Patino-Navarrete et al, 2014). Such bacteria are commonly harbored in bacteriocytes, specialized host cells that sometimes form special organ-like structures, the bacteriomes (Baumann, 2005) or are confined to the insect gut (Engel and Moran, 2013).…”