Serratia symbiotica from the aphid Cinara cedri: a missing link from facultative to obligate insect endosymbiont - PubMed (original) (raw)

Araceli Lamelas et al. PLoS Genet. 2011 Nov.

Abstract

The genome sequencing of Buchnera aphidicola BCc from the aphid Cinara cedri, which is the smallest known Buchnera genome, revealed that this bacterium had lost its symbiotic role, as it was not able to synthesize tryptophan and riboflavin. Moreover, the biosynthesis of tryptophan is shared with the endosymbiont Serratia symbiotica SCc, which coexists with B. aphidicola in this aphid. The whole-genome sequencing of S. symbiotica SCc reveals an endosymbiont in a stage of genome reduction that is closer to an obligate endosymbiont, such as B. aphidicola from Acyrthosiphon pisum, than to another S. symbiotica, which is a facultative endosymbiont in this aphid, and presents much less gene decay. The comparison between both S. symbiotica enables us to propose an evolutionary scenario of the transition from facultative to obligate endosymbiont. Metabolic inferences of B. aphidicola BCc and S. symbiotica SCc reveal that most of the functions carried out by B. aphidicola in A. pisum are now either conserved in B. aphidicola BCc or taken over by S. symbiotica. In addition, there are several cases of metabolic complementation giving functional stability to the whole consortium and evolutionary preservation of the actors involved.

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Conflict of interest statement

The authors have declared that no competing interests exist.

Figures

Figure 1

Figure 1. Inferred metabolism of amino acids, nucleotides, membrane compounds, cofactors, and vitamins of the _C. cedri_-consortium.

B. aphidicola BCc is represented by three concentric black rectangles and S. symbiotica SCc by three red ones. The two internal rectangles represent internal and external bacterial membranes and the external rectangle represents the vesicle of the eukaryotic cell. The two blue lines represent the membrane in the bacteriocytes. Metabolites are black when synthesized, grey when not synthesized, red when their synthesis is not clear, and green for intermediates exchanged between partners. Black lines indicate intact pathways. Blue, pink and green squares on the membranes represent transporters (red indicating non-functional system). Orange boxes correspond to secretion systems.

Figure 2

Figure 2. Outline of the putative synthesis of nucleotides by the consortium (C. cedri, B. aphidicola BCc, and S. symbiotica SCc).

The number of genes involved in each pathway is shown as black circles beside them. The intermediate metabolites are colored in green. Green arrows indicate the movement of intermediary metabolites. In the case of aphid, the genes are postulated.

Figure 3

Figure 3. Outline of the putative synthesis of the amino acids serine, cysteine, isoleucine, and methionine by the consortium (C. cedri, B. aphidicola BCc, and S. symbiotica SCc).

Rest as in Figure 2.

Figure 4

Figure 4. Outline of the putative synthesis of fatty acids, phospholipids (cardiolipin, phosphatidyl-ethanolamine, dyacilglycerol prolipoprotein), peptidoglycan, and lipopolysaccharide by the consortium (C. cedri, B. aphidicoa BCc, and S. symbiotica SCc).

White circles representing absent genes. Rest as in Figure 2.

Figure 5

Figure 5. Synteny plots.

Dot plots displaying syinteny between different species of Serratia in the shared groups of genes. (A) S. proteamaculans is taken as reference against S. odorifera. (B) S. proteamaculans is taken as reference against S. symbiotica SAp. (C) S. symbiotica SCc is taken as reference against S. proteamaculans and (D) S. symbiotica SCc is taken as reference against S. symbiotica SAp. Red dots, direct match; blue dots, reverse match.

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