Abstract
Insects with restricted diets rely on obligate microbes to fulfil nutritional requirements essential for biological function. Tsetse flies, vectors of African trypanosome parasites, feed exclusively on vertebrate blood and harbour the obligate endosymbiont Wigglesworthia glossinidia. Without Wigglesworthia, tsetse are unable to reproduce. These symbionts are sheltered within specialized cells (bacteriocytes) that form the midgut-associated bacteriome organ. To decipher the core functions of this symbiosis essential for tsetse's survival, we performed dual-RNA-seq analysis of the bacteriome, coupled with metabolomic analysis of bacteriome and haemolymph collected from normal and symbiont-cured (sterile) females. Bacteriocytes produce immune regulatory peptidoglycan recognition protein (pgrp-lb) that protects Wigglesworthia, and a multivitamin transporter (smvt) that can aid in nutrient dissemination. Wigglesworthia overexpress a molecular chaperone (GroEL) to augment their translational/transport machinery and biosynthesize an abundance of B vitamins (specifically B1-, B2-, B3- and B6-associated metabolites) to supplement the host's nutritionally deficient diet. The absence of Wigglesworthia's contributions disrupts multiple metabolic pathways impacting carbohydrate and amino acid metabolism. These disruptions affect the dependent downstream processes of nucleotide biosynthesis and metabolism and biosynthesis of S-adenosyl methionine (SAM), an essential cofactor. This holistic fundamental knowledge of the symbiotic dialogue highlights new biological targets for the development of innovative vector control methods.
Highlights
The nature of symbiotic associations between microorganisms and animals range from mutualistic to parasitic interactions [1]
Pea aphids rely on Buchnera aphidicola for essential amino acids low in plant phloem [4], while tsetse obtain specific blood-deficient nutrients from Wigglesworthia glossinidia [5,6]
As rRNAs account for over 80% of cellular RNA, sequencing of total RNA without mRNA enrichment yields mostly non-mRNA sequences [21,22]. This issue is exacerbated when measuring gene expression of obligate intracellular symbionts residing in host tissues, and typically yields a low proportion of bacterial RNAs
Summary
The nature of symbiotic associations between microorganisms and animals range from mutualistic to parasitic interactions [1]. Despite this genomic reduction, the small genome of Buchnera (about 445 kb in size) has retained the ability to synthesize all essential amino acids [7,8], while the genome of Wigglesworthia (about 700 kb in size) encodes the enzymes of pathways involved in the synthesis of many B vitamins [9,10]. Differential expression of Wigglesworthia genes have been noted from the bacteriome organ and the female milk, such as those that encode flagella-associated proteins which are produced only by extracellular Wigglesworthia [9], and may facilitate symbiont transmission to the larva [9,15]. Wigglesworthia is required for tsetse’s fecundity, as without this bacterium females are unable to support the development of their intrauterine larva. We discuss the core functions of the obligate symbiosis and the host physiological pathways dependent on this relationship to maintain the optimal host and symbiont homeostasis
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