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Mtor Complex 1 Implicated in Aphid/Buchnera Host/Symbiont Integration

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Mtor Complex 1 Implicated in Aphid/Buchnera Host/Symbiont Integration G3: Genes|Genomes|Genetics Early Online, published on July 26, 2018 as doi:10.1534/g3.118.200398 1 mTOR complex 1 implicated in aphid/Buchnera host/symbiont integration 2 3 Edward B. James, Honglin Feng, & Alex C. C. Wilson 4 Department of Biology, University of Miami, Coral Gables, FL 33146 USA 5 6 © The Author(s) 2013. Published by the Genetics Society of America. 7 Running Title: Aphid mTOR 8 9 Keywords: mTORC1, symbiosis, Myzus persicae, transcriptome 10 11 Corresponding author: 12 Dr. Alex C. C. Wilson 13 Department of Biology 14 1301 Memorial Drive 15 Coral Gables, FL 33146 16 USA 17 (305) 284-2003 18 [email protected] 19 ABSTRACT 20 Obligate nutritional endosymbioses are arguably the most intimate of all interspecific 21 associations. While many insect nutritional endosymbioses are well studied, a full picture 22 of how two disparate organisms, a bacterial endosymbiont and a eukaryotic host, are 23 integrated is still lacking. The mTOR pathway is known to integrate nutritional conditions 24 with cell growth and survival in eukaryotes. Characterization and localization of amino acid 25 transporters in aphids suggest the mTOR pathway as point of integration between an aphid 26 host and its amino acid-provisioning endosymbiont Buchnera aphidicola. The mTOR 27 pathway is unannotated in aphids and unstudied in any nutritional endosymbiosis. We 28 annotated mTOR pathway genes in two aphid species, Acyrthosiphon pisum and Myzus 29 persicae, using both BLASTp searches and Hidden Markov Models. Using previously 30 collected RNAseq data we constructed new reference transcriptomes for bacteriocyte, gut, 31 and whole insect tissue for three lines of M. persicae. Annotation of the mTOR pathway 32 identified homologs of all known invertebrate mTOR genes in both aphid species with 33 some duplications. Differential expression analysis showed that genes specific to the amino 34 acid-sensitive mTOR Complex 1 were more highly expressed in bacteriocytes than genes 35 specific to the amino acid-insensitive mTOR Complex 2. Almost all mTOR genes involved in 36 sensing amino acids showed higher expression in bacteriocytes than in whole insect tissue. 37 When compared to gut, the putative glutamine/arginine sensing transporter ACYPI000333, 38 an ortholog of SLC38A9, showed 6.5 times higher expression in bacteriocytes. Our results 39 suggest that the mTOR pathway may be functionally important in mediating integration of 40 Buchnera into aphid growth and reproduction. 41 INTRODUCTION 42 Two species living together in symbiosis can reciprocally impact each other’s evolution 43 (Ehrlich and Raven 1964). The most intimate symbioses are those where one species 44 resides inside the cells of the second species in obligate endosymbiosis (Wernegreen 45 2004). In plant-sap feeding insects such obligate endosymbioses are typically nutritional 46 and feature hosts that require their endosymbiont for reproduction, and endosymbionts 47 that are unable to survive outside their host. Despite the apparent harmony between 48 members of these nutritional endosymbioses the partners must balance conflict and 49 cooperation for the relationship to persist (Bennett and Moran 2015; Wernegreen 2004). 50 The host must not completely reject the intracellular symbiont population but instead must 51 provision the metabolites required for endosymbiont survival. In turn, the endosymbiont 52 must persist within the host cell without imposing a fatal cost upon the host. Members of 53 an endosymbiosis face unique and separate selection pressures that govern their evolution 54 as discrete species, while existing in a robust state of integration (Bennett and Moran 2015; 55 Keeling and McCutcheon 2017). Despite the evolutionary, ecological, agricultural and 56 economic importance of many insect obligate nutritional endosymbioses a full picture of 57 how these relationships are functionally regulated by their members is lacking. Therefore 58 an understanding of how these endosymbiotic interactions evolved, are maintained, and 59 indeed how they might be targeted for human control is also wanting. 60 The most-studied insect model of a host endosymbiont relationship is that of aphids 61 and their endosymbiont, Buchnera aphidicola. Buchnera are housed within specialized 62 aphid organs called bacteriomes, where they are contained inside bacteriocyte cells 63 (Baumann et al. 1995). The two species are integrated to such an extent that Buchnera is 64 unable to produce their own outer-membrane, and instead it is assumed to be produced by 65 the aphid host (Shigenobu et al. 2000). Another feature of the integration includes the loss 66 in both aphid hosts and Buchnera of amino acid biosynthesis genes. Such gene losses have 67 sometimes involved the complete degradation of pathways like the TCA cycle in Buchnera, 68 (rendering Buchnera incapable of producing glutamate and aspartate), and the urea cycle 69 in aphids (rendering aphids incapable of producing arginine) (International Aphid 70 Genomics 2010; Shigenobu et al. 2000). Other times gene losses have not eliminated a 71 pathway but rather fragmented it in such a way that completion of the metabolic pathway 72 requires the contribution of enzymes encoded by genes in both the host and the symbiont 73 genome (Hansen and Moran 2011; Price et al. 2015; Wilson et al. 2010). 74 Multiple points of regulation of the collaborative biosynthesis of amino acids in 75 aphids have recently been identified. First, Buchnera’s amino acid production has been 76 proposed to be in part regulated by host-controlled supply of the precursor glutamine via a 77 glutamine specific amino-acid transporter which is highly expressed in bacteriocytes and 78 competitively inhibited by arginine, a Buchnera produced end-product amino acid (Price et 79 al. 2014; Price et al. 2015). Second, microbial small RNAs that are conserved across 80 Buchnera from different aphid species have been proposed to function in Buchnera gene 81 regulation (Hansen and Degnan 2014). In particular, life-stage dependent differential 82 expression of amino acid biosynthesis pathways within Buchnera has been hypothesized to 83 result from post-transcriptional small RNA regulation within Buchnera (Hansen and 84 Degnan 2014). Third, microRNAs (miRNAs) encoded in aphid genomes have been found to 85 show bacteriocyte-specific expression (Feng et al. 2017). Remarkably, of the 14 miRNAs 86 highly or differentially expressed within aphid bacteriocytes, ten have previously been 87 characterized to play roles in host/microbe interactions (Feng et al. 2017). The emerging 88 picture of host/endosymbiont regulation is one of multiple concurrent and overlapping 89 mechanisms of integration. While some of these mechanisms have been characterized we 90 do not yet have a full mechanistic understanding of host/endosymbiont integration. In 91 particular, the mechanisms that link Buchnera amino acid output, the currency of this 92 nutritional endosymbiotic relationship, to symbiont growth and proliferation are yet to be 93 identified. 94 The highly conserved mechanistic target of rapamycin (mTOR) signaling pathway 95 (fig. 1) links a cell’s intracellular amino acid availability, extracellular growth factors, and 96 available energy levels to cellular responses that include protein synthesis, lipid synthesis, 97 cell proliferation, cytoskeleton organization, autophagy, and mitochondrial regulation and 98 proliferation (Crespo and Hall 2002; Laplante and Sabatini 2012; Morita et al. 2015; 99 Sarbassov et al. 2004; Shimobayashi and Hall 2016; Goberdhan et al. 2016). This signaling 100 pathway centers around two complexes: mTOR complex 1 (mTORC1) and mTOR complex 2 101 (mTORC2). The complexes form around the mTOR protein, but differ in protein 102 composition such that each complex has distinct functions. mTORC1 is activated in 103 response to sufficient levels of amino acids and responds by signaling for protein, 104 nucleotide and lipid synthesis, and blocking autophagy; mTORC1 allows cellular growth 105 when nutritional conditions will support growth (Goberdhan et al. 2016). The genes and 106 complexes upstream of mTORC1 and mTORC1 itself are referred to in this paper as the 107 amino acid sensing pathway. In contrast, mTORC2 integrates growth factors and other 108 extracellular signals with cell survival and cytoskeleton organization (Ebner et al. 2017; 109 Wullschleger et al. 2006). The mTOR pathway represents a conspicuous candidate for 110 integrating amino acid-provisioning, endosymbiont growth and population size to their 111 metabolic output within host tissues. Currently, mTOR is unannotated and unstudied in any 112 nutritional endosymbiosis. 113 114 In this study we present an annotation of the central components of the mTOR 115 pathway and its associated amino acid sensing cellular machinery in the aphids Myzus 116 persicae and Acyrthosiphon pisum. In addition, we re-analyze previously collected RNAseq 117 data generated from M. persicae bacteriome, gut, and whole insect tissue reporting 118 differential and ranked expression of mTOR pathway components from three genetically 119 distinct M. persicae lines. 120 MATERIALS AND METHODS 121 Annotation of the mTOR pathway in Myzus persicae and Acyrthosiphon pisum was done 122 using both BLASTp searches in which annotated mTOR proteins from Drosophila 123 melanogaster were used as queries (accessed from FlyBase), and Hidden Markov Models of 124 mTOR-associated genes (accessed from PantherDB) against the M. persicae G006 (NCBI 125 taxid: 13164) and A.
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