This publication has been written with the support of the AgreenSkillsþ fellowship program that has received funding from the EU's Seventh Framework Programme under grant agreement N FP7-609398 (AgreenSkillsþ contract). We are grateful to the genotoul bioinformatics platform Toulouse Midi-Pyrenees (Bioinfo Genotoul) for providing help and/or computing and/or storage resources. The authors are grateful to the CBGP-HPC computational platform. The funders had no role in study design, AgreenSkillsþ fellowship program cofunded by the EU's Seventh Framework Programme (FP7-609398) to A.M.M., the Agropolis foundation/Labex Agro ,
Symbiotic bacteria enable insect to use a nutritionally inadequate diet, Proc R Soc Lond B Biol Sci, vol.276, pp.987-991, 1658. ,
Gapped BLAST and PSI-BLAST: a new generation of protein database search programs, Nucleic Acids Res, vol.25, issue.17, pp.3389-3402, 1997. ,
Small genome symbiont underlies cuticle hardness in beetles, Proc Natl Acad Sci U S A, vol.114, issue.40, pp.8382-8391, 2017. ,
Studies on the symbiosis of the body louse: I. Elimination of the symbionts by centrifugalisation of the eggs, Parasitology, vol.26, issue.03, pp.309-314, 1934. ,
SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing, J Comput Biol, vol.19, issue.5, pp.455-477, 2012. ,
Small, smaller, smallest: the origins and evolution of ancient dual symbioses in a phloem-feeding insect, 2013. ,
, Genome Biol Evol, vol.5, issue.9, pp.1675-1688
Aphids on the world's trees: an identification and information guide, CAB International, Natural History Museum, 1994. ,
Domain enhanced lookup time accelerated BLAST, Biol Direct, vol.7, p.12, 2012. ,
Genome-scale evolution: reconstructing gene orders in the ancestral species, Genome Res, vol.12, issue.1, pp.26-36, 2002. ,
, Endosymbiose der Tiere mit Pflanzlichen Mikroorganismen. Basel: Birkh? auser, 1953.
Massive genomic decay in Serratia symbiotica, a recently evolved symbiont of aphids, Genome Biol Evol, vol.3, issue.0, pp.195-208, 2011. ,
Evolution and diversity of facultative symbionts from the aphid subfamily Lachninae, Appl Environ Microbiol, vol.75, issue.16, pp.5328-5335, 2009. ,
BLASTþ: architecture and applications, BMC Bioinformatics, vol.10, p.421, 2009. ,
Physical and genetic map of the genome of Buchnera, the primary endosymbiont of the pea aphid Acyrthosiphon pisum, J Mol Evol, vol.48, issue.2, pp.142-150, 1999. ,
Assessing performance of orthology detection strategies applied to eukaryotic genomes, PLoS ONE, vol.2, issue.4, p.383, 2007. ,
Evolutionary loss and replacement of Buchnera, the obligate endosymbiont of aphids, ISME J, vol.12, issue.3, pp.898-908, 2018. ,
A novel human-infection-derived bacterium provides insights into the evolutionary origins of mutualistic insectbacterial symbioses, PLoS Genet, vol.8, issue.11, p.1002990, 2012. ,
Genome sequence of Blochmannia pennsylvanicus indicates parallel evolutionary trends among bacterial mutualists of insects, Genome Res, vol.15, issue.8, pp.1023-1033, 2005. ,
Dynamics of genome evolution in facultative symbionts of aphids, Environ Microbiol, vol.12, issue.8, pp.2060-2069, 2010. ,
Sequence conservation and functional constraint on intergenic spacers in reduced genomes of the obligate symbiont Buchnera, PLoS Genet, vol.7, issue.9, p.1002252, 2011. ,
Hamiltonella defensa, genome evolution of protective bacterial endosymbiont from pathogenic ancestors, Proc Natl Acad Sci U S A, vol.106, issue.22, pp.9063-9068, 2009. ,
Reproductive failure and the free amino acid pools in pea aphids (Acyrthosiphon pisum) lacking symbiotic bacteria, J Insect Physiol, vol.42, issue.3, pp.247-255, 1996. ,
UCHIME improves sensitivity and speed of chimera detection, Bioinformatics, vol.27, issue.16, pp.2194-2200, 2011. ,
The genome sequence of Blochmannia floridanus: comparative analysis of reduced genomes, Proc Natl Acad Sci U S A, vol.100, issue.16, pp.9388-9393, 2003. ,
Ultrastructure of pea aphid mycetocytes: evidence for symbiote secretion, Cell Tissue Res, vol.159, issue.3, pp.351-367, 1975. ,
Aphid genome expression reveals hostsymbiont cooperation in the production of amino acids, Proc Natl Acad Sci U S A, vol.108, issue.7, pp.2849-2854, 2011. ,
Strict hostsymbiont cospeciation and reductive genome evolution in insect gut bacteria, PLoS Biol, vol.4, issue.10, p.337, 2006. ,
Genome sequence of Blattabacterium sp. strain BGIGA, Endosymbiont of the Blaberus giganteus Cockroach, J Bacteriol, vol.194, issue.16, pp.4450-4451, 2012. ,
Multiple origins of endosymbiosis within the Enterobacteriaceae (c-Proteobacteria): convergence of complex phylogenetic approaches, BMC Biol, vol.9, issue.1, p.87, 2011. ,
Repeated replacement of an intrabacterial symbiont in the tripartite nested mealybug symbiosis, Proc Natl Acad Sci U S A, vol.113, issue.37, pp.5416-5424, 2016. ,
Assessment of a 16S rRNA amplicon Illumina sequencing procedure for studying the microbiome of a symbiontrich aphid genus, Mol Ecol Resour, vol.16, issue.3, pp.628-640, 2016. ,
URL : https://hal.archives-ouvertes.fr/hal-01449134
Complete genome sequence of the endosymbiont Blattabacterium from the cockroach Nauphoeta cinerea (Blattodea: blaberidae), Genomics, vol.102, issue.5-6, pp.479-483, 2013. ,
MAFFT Multiple Sequence Alignment Software Version 7: improvements in performance and usability, Mol Biol Evol, vol.30, issue.4, pp.772-780, 2013. ,
A novel intracellular mutualistic bacterium in the invasive ant Cardiocondyla obscurior, ISME J, vol.10, issue.2, pp.376-388, 2016. ,
Swapping symbionts in spittlebugs: evolutionary replacement of a reduced genome symbiont, ISME J, vol.8, issue.6, pp.1237-1246, 2014. ,
Changing partners in an obligate symbiosis: a facultative endosymbiont can compensate for loss of the essential endosymbiont Buchnera in an aphid, Proc R Soc Lond B Biol Sci, vol.270, pp.2543-2550, 1533. ,
Development of a dual-index sequencing strategy and curation pipeline for analyzing amplicon sequence data on the MiSeq Illumina Sequencing Platform, Appl Environ Microbiol, vol.79, issue.17, pp.5112-5120, 2013. ,
Serratia symbiotica from the aphid Cinara cedri: a missing link from facultative to obligate insect endosymbiont, PLoS Genet, vol.7, issue.11, p.1002357, 2011. ,
New clues about the evolutionary history of metabolic losses in bacterial endosymbionts, provided by the genome of Buchnera aphidicola from the aphid Cinara tujafilina, Appl Environ Microbiol, vol.77, issue.13, pp.4446-4454, 2011. ,
Candidatus Serratia symbiotica" in Aphid Species of the Subfamily Lachninae, Appl Environ Microbiol, vol.74, issue.13, pp.4236-4240, 2008. ,
PhyloBayes 3: a Bayesian software package for phylogenetic reconstruction and molecular dating, Bioinformatics, vol.25, issue.17, pp.2286-2288, 2009. ,
ARAGORN, a program to detect tRNA genes and tmRNA genes in nucleotide sequences, Nucleic Acids Res, vol.32, issue.1, pp.11-16, 2004. ,
Dissecting genome reduction and trait loss in insect endosymbionts, Ann N Y Acad Sci, vol.1389, issue.1, pp.52-75, 2017. ,
An improved general amino acid replacement matrix, Mol Biol Evol, vol.25, issue.7, pp.1307-1320, 2008. ,
URL : https://hal.archives-ouvertes.fr/lirmm-00324106
OrthoMCL: identification of ortholog groups for eukaryotic genomes, Genome Res, vol.13, issue.9, pp.2178-2189, 2003. ,
Evolutionary convergence and nitrogen metabolism in Blattabacterium strain Bge, primary endosymbiont of the cockroach Blattella germanica, PLoS Genet, vol.5, issue.11, p.1000721, 2009. ,
tRNAscan-SE On-line: integrating search and context for analysis of transfer RNA genes, Nucleic Acids Res, vol.44, issue.W1, pp.54-57, 2016. ,
Settling Down: the Genome of Serratia symbiotica from the Aphid Cinara tujafilina Zooms in on the process of accommodation to a cooperative intracellular life, Genome Biol Evol, vol.6, issue.7, pp.1683-1698, 2014. ,
Snapshots of a shrinking partner: genome reduction in Serratia symbiotica, Sci Rep, vol.6, p.32590, 2016. ,
Solving a bloody mess: b-vitamin independent metabolic convergence among gammaproteobacterial obligate endosymbionts from blood-feeding arthropods and the Leech Haementeria officinalis, Genome Biol Evol, vol.7, issue.10, pp.2871-2884, 2015. ,
Reinventing the wheel and making it round again: evolutionary convergence in Buchnera -Serratia symbiotic Consortia between the distantly related Lachninae Aphids Tuberolachnus salignus and Cinara cedri, Genome Biol Evol, vol.8, issue.5, pp.1440-1458, 2016. ,
Happens in the best of subfamilies: establishment and repeated replacements of co-obligate secondary endosymbionts within Lachninae aphids, Environ Microbiol, vol.19, issue.1, pp.393-408, 2017. ,
, DNA mismatch repair. EcoSal Plus, vol.5, issue.1, 2012.
Functional convergence in reduced genomes of bacterial symbionts spanning 200 million years of evolution, Genome Biol Evol, vol.2, pp.708-718, 2010. ,
Extreme genome reduction in symbiotic bacteria, Nat Rev Microbiol, vol.10, issue.1, pp.13-26, 2011. ,
Buchnera has changed flatmate but the repeated replacement of co-obligate symbionts is not associated with the ecological expansions of their aphid hosts, Mol Ecol, vol.26, issue.8, pp.2363-2378, 2017. ,
URL : https://hal.archives-ouvertes.fr/hal-02623952
Some effects on the aphid Myzus persicae of ingesting antibiotics incorporated into artificial diets, J Insect Physiol, vol.17, issue.7, pp.1333-1347, 1971. ,
Taxonomic classification of bacterial 16S rRNA genes using short sequencing reads: evaluation of effective study designs, PLoS One, vol.8, issue.1, p.53608, 2013. ,
Accelerated evolution and Muller's rachet in endosymbiotic bacteria, Proc Natl Acad Sci U S A, vol.93, issue.7, pp.2873-2878, 1996. ,
The tiniest tiny genomes, Annu Rev Microbiol, vol.68, pp.195-215, 2014. ,
Regulation of transcription in a reduced bacterial genome: nutrient-provisioning genes of the obligate symbiont Buchnera aphidicola, J Bacteriol, vol.187, issue.12, pp.4229-4237, 2005. ,
Genomics and evolution of heritable bacterial symbionts, Annu Rev Genet, vol.42, pp.165-190, 2008. ,
Genomic changes following host restriction in bacteria, Curr Opin Genet Dev, vol.14, issue.6, pp.627-633, 2004. ,
Buchnera gen.nov. and Buchnera aphidicola sp. nov., a Taxon Consisting of the Mycetocyte-Associated, Primary Endosymbionts of Aphids, Int J Syst Bacteriol, vol.41, issue.4, pp.566-568, 1991. ,
Provision of riboflavin to the host aphid, Acyrthosiphon pisum, by endosymbiotic bacteria, Buchnera. J Insect Physiol, vol.45, issue.1, pp.1-6, 1999. ,
Rfam 12.0: updates to the RNA families database, Nucleic Acids Res, vol.43, pp.130-137, 2015. ,
Infernal 1.1: 100-fold faster RNA homology searches, Bioinformatics, vol.29, issue.22, pp.2933-2935, 2013. ,
Evolutionary origin of insect-Wolbachia nutritional mutualism, Proc Natl Acad Sci U S A, vol.111, issue.28, pp.10257-10262, 2014. ,
Sterility in tsetse flies (Glossina morsitans Westwood) caused by loss of symbionts, Experientia, vol.32, issue.8, pp.995-996, 1976. ,
Significance of symbionts for the maintenance of an optimal nutritional state for successful reproduction in haematophagous arthropods, Parasitology, vol.82, issue.4, pp.101-104, 1981. ,
Reconstructing the phylogeny of aphids (Hemiptera: aphididae) using DNA of the obligate symbiont Buchnera aphidicola, Mol Phylogenet Evol, vol.68, issue.1, pp.42-54, 2013. ,
Genome degeneration and adaptation in a nascent stage of symbiosis, Genome Biol Evol, vol.6, issue.1, pp.76-93, 2014. ,
URL : https://hal.archives-ouvertes.fr/hal-01449146
Effects of heat treatment on the symbiotic system of an aphid mycetocyte, Symbiosis, vol.11, pp.19-30, 1991. ,
Unipro UGENE: a unified bioinformatics toolkit, Bioinformatics, vol.28, issue.8, pp.1166-1167, 2012. ,
Comparative genomics of Blattabacterium cuenoti: the Frozen Legacy of an Ancient Endosymbiont Genome, Genome Biol Evol, vol.5, issue.2, pp.351-361, 2013. ,
A small microbial genome: the end of a long symbiotic relationship?, Science, vol.314, issue.5797, pp.312-313, 2006. ,
Difficult phylogenetic questions: more data, maybe; better methods, certainly, BMC Biol, vol.9, issue.1, p.91, 2011. ,
Large-scale label-free quantitative proteomics of the pea aphid-Buchnera symbiosis, Mol Cell Proteomics, vol.10, issue.6, 2011. ,
The SILVA ribosomal RNA gene database project: improved data processing and web-based tools, Nucleic Acids Res. 41(Database issue, pp.590-596, 2013. ,
Insight into the transmission biology and speciesspecific functional capabilities of Tsetse (Diptera: glossinidae) obligate symbiont Wigglesworthia, mBio, vol.3, issue.1, pp.240-00211, 2012. ,
MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space, Syst Biol, vol.61, issue.3, pp.539-542, 2012. ,
Shared metabolic pathways in a coevolved insect-bacterial symbiosis, Appl Environ Microbiol, vol.79, p.6117, 2013. ,
Matching the supply of bacterial nutrients to the nutritional demand of the animal host, Proc R Soc Lond B Biol Sci, vol.281, p.20141163, 1791. ,
Nitrogen recycling and nutritional provisioning by Blattabacterium, the cockroach endosymbiont, Proc Natl Acad Sci U S A, vol.106, pp.19521-19526, 2009. ,
Effects of heat treatment on the symbiotic system of Blattoidea: morphofunctional alterations of bacteriocytes, Boll Zool, vol.60, issue.3, pp.271-279, 1993. ,
How nutritionally imbalanced is phloem sap for aphids, Entomol Exp Appl, vol.91, issue.1, pp.203-210, 1999. ,
Assessing and improving methods used in operational taxonomic unit-based approaches for 16S rRNA gene sequence analysis, Appl Environ Microbiol, vol.77, issue.10, pp.3219-3226, 2011. ,
Quality control and preprocessing of metagenomic datasets, Bioinformatics, vol.27, issue.6, pp.863-864, 2011. ,
Genome sequence of the endocellular bacterial symbiont of aphids Buchnera sp, Nature, vol.407, issue.6800, pp.81-86, 2000. ,
A probabilistic method for identifying start codons in bacterial genomes, Bioinformatics, vol.17, issue.12, pp.1123-1130, 2001. ,
Convergent patterns in the evolution of mealybug symbioses involving different intrabacterial symbionts, ISME J, vol.11, issue.3, pp.715-726, 2017. ,
Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments, Syst Biol, vol.56, issue.4, pp.564-577, 2007. ,
50 million years of genomic stasis in endosymbiotic bacteria, Science, vol.296, issue.5577, pp.2376-2379, 2002. ,
Maintenance of essential amino acid synthesis pathways in the Blattabacterium cuenoti symbiont of a woodfeeding cockroach, Biol Lett, vol.9, issue.3, p.20121153, 2013. ,
BASys: a web server for automated bacterial genome annotation, Nucleic Acids Res, vol.33, pp.455-459, 2005. ,
Reductive genome evolution in Buchnera aphidicola, Proc Natl Acad Sci U S A, vol.100, issue.2, pp.581-586, 2003. ,
Functional and evolutionary analysis of the genome of an obligate fungal symbiont, Genome Biol Evol, vol.5, issue.5, pp.891-904, 2013. ,
M-Coffee: combining multiple sequence alignment methods with T-Coffee, Nucleic Acids Res, vol.34, issue.6, pp.1692-1699, 2006. ,
Naïve Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy, Appl Environ Microbiol, vol.73, issue.16, pp.5261-5267, 2007. ,
Genome evolution in an ancient bacteria-ant symbiosis: parallel gene loss among Blochmannia spanning the origin of the ant tribe Camponotini, PeerJ, vol.3, p.881, 2015. ,
Nature of Transported Substances, Encyclopedia of plant physiology, vol.1, pp.59-100, 1975. ,