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The Cost of Metabolic Interactions in Symbioses Between Insects and Bacteria With Reduced Genomes

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The Cost of Metabolic Interactions in Symbioses Between Insects and Bacteria With Reduced Genomes

Nana Y D Ankrah et al. mBio.

Abstract

Various intracellular bacterial symbionts that provide their host with essential nutrients have much-reduced genomes, attributed largely to genomic decay and relaxed selection. To obtain quantitative estimates of the metabolic function of these bacteria, we reconstructed genome- and transcriptome-informed metabolic models of three xylem-feeding insects that bear two bacterial symbionts with complementary metabolic functions: a primary symbiont, Sulcia, that has codiversified with the insects, and a coprimary symbiont of distinct taxonomic origin and with different degrees of genome reduction in each insect species (Hodgkinia in a cicada, Baumannia in a sharpshooter, and Sodalis in a spittlebug). Our simulations reveal extensive bidirectional flux of multiple metabolites between each symbiont and the host, but near-complete metabolic segregation (i.e., near absence of metabolic cross-feeding) between the two symbionts, a likely mode of host control over symbiont metabolism. Genome reduction of the symbionts is associated with an increased number of host metabolic inputs to the symbiont and also reduced metabolic cost to the host. In particular, Sulcia and Hodgkinia with genomes of ≤0.3 Mb are calculated to recycle ∼30 to 80% of host-derived nitrogen to essential amino acids returned to the host, while Baumannia and Sodalis with genomes of ≥0.6 Mb recycle 10 to 15% of host nitrogen. We hypothesize that genome reduction of symbionts may be driven by selection for increased host control and reduced host costs, as well as by the stochastic process of genomic decay and relaxed selection.IMPORTANCE Current understanding of many animal-microbial symbioses involving unculturable bacterial symbionts with much-reduced genomes derives almost entirely from nonquantitative inferences from genome data. To overcome this limitation, we reconstructed multipartner metabolic models that quantify both the metabolic fluxes within and between three xylem-feeding insects and their bacterial symbionts. This revealed near-complete metabolic segregation between cooccurring bacterial symbionts, despite extensive metabolite exchange between each symbiont and the host, suggestive of strict host controls over the metabolism of its symbionts. We extended the model analysis to investigate metabolic costs. The positive relationship between symbiont genome size and the metabolic cost incurred by the host points to fitness benefits to the host of bearing symbionts with small genomes. The multicompartment metabolic models developed here can be applied to other symbioses that are not readily tractable to experimental approaches.

Keywords: constraint-based modeling; flux balance analysis; nitrogen recycling; symbiosis; xylem-feeding insects.

Figures

FIG 1
FIG 1
Metabolic interactions in xylem-feeding insect-bacterial symbiosis. (a to c) The insects used in this study (a) spittlebug (Philaenus spumarius), (b) sharpshooter (Graphocephala coccinea), and (c) cicada (Neotibicen canicularis). (d to F) Model structure showing species compartments and metabolites exchanged between each compartment for (d) spittlebug, (e) sharpshooter, and (f) cicada symbiosis. Bacterial genome size and the total number of metabolites in each compartment are shown in parentheses. The number of input and output metabolites for each compartment is displayed alongside the arrows. (g and h) Metabolic network maps of integrated three-partner (g) spittlebug, (h) sharpshooter, and (i) cicada models. The prefuse force-directed algorithm was used for generating the network layout and visualized with Cytoscape_v3.4.0. Circles (gold, red, and black) represent metabolites, and squares (brown, blue, and green) represent reactions.
FIG 2
FIG 2
Comparison of EAA synthesis fluxes and utilization profiles for three-compartment insect-bacterial symbioses. (a to c) In silico predictions of EAA export by bacteria in sharpshooter, cicada, and spittlebug symbiosis. (d to f) Comparison of EAA utilization profiles for bacteria and host in (d) sharpshooter, (e) cicada, and (f) spittlebug symbiosis. (g) In silico predictions of EAA production in sharpshooter, cicada, and spittlebug symbiosis.
FIG 3
FIG 3
Comparison of metabolites exported by bacteria from three-compartment insect-bacterial symbioses based on metabolite counts and metabolite fluxes. (a) Relationship between bacterial genome size and number of metabolic outputs exported to the host. (b to e) Metabolic outputs to bacterial compartments based on (b and c) metabolite counts and (d and e) metabolite fluxes. (Note the difference in scales of flux between the primary symbionts [left] and coprimary symbionts [right].) Fluxes of individual metabolite production and consumption are provided in Table S1e to g.
FIG 4
FIG 4
Metabolite cross-feeding between bacterial partners. Shown are metabolites exchanged exclusively between bacterial partners in (a) spittlebug, (b) sharpshooter, and (c) cicada symbiosis. Metabolites produced by Sulcia are colored red. Inferred fluxes for metabolite groups assimilated and released by bacteria are given in mmol g dry weight−1 h−1.
FIG 5
FIG 5
Comparison of metabolites consumed by bacteria from three-compartment insect-bacterial symbioses based on metabolite counts and metabolite fluxes. Shown are metabolic inputs to bacterial compartments based on (a and b) metabolite counts and (c and d) metabolite fluxes. (Note the difference in scales of flux between the primary symbionts [left] and coprimary symbionts [right].) (e) Relationship between bacterial genome size and number of metabolic inputs derived from the host. Fluxes of individual metabolite production and consumption are provided in Table S1e to g.
FIG 6
FIG 6
Bacterial maintenance costs incurred by host insects. Bacterial maintenance costs are inferred from reductions in growth flux the host incurs by harboring a bacterium.
FIG 7
FIG 7
Nitrogen utilization by bacterial symbionts. Inferred fluxes for total nitrogen assimilated and released by bacteria are calculated by multiplying the flux through a metabolite transport reaction by the N stoichiometry of the given metabolite. (a) Spittlebug. (b) Sharpshooter. (c) Cicada. Broken arrows represent transport fluxes between host and symbionts. Reaction fluxes (mmol g dry weight−1 h−1) are shown below each metabolite transport class. Percentages represent the proportion of flux through each metabolite transport class (e.g., non-EAA transport input flux) relative to the total N input transport flux into each symbiotic partner (denoted by bold text with an asterisk). Individual metabolite fluxes are shown in Table S1i.

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