Section: Evolutionary Biology
Topic: Evolution, Biology of interactions
Co-obligate symbioses have repeatedly evolved across aphids, but partner identity and nutritional contributions vary across lineages
10.24072/pcjournal.278 - Peer Community Journal, Volume 3 (2023), article no. e46.
Get full text PDF Peer reviewed and recommended by PCI
Aphids are a large family of phloem-sap feeders. They typically rely on a single bacterial endosymbiont, Buchnera aphidicola, to supply them with essential nutrients lacking in their diet. This association with Buchnera was described in model aphid species from the Aphidinae subfamily and has been assumed to be representative of most aphids. However, in two lineages, Buchnera has lost some essential symbiotic functions and is now complemented by additional symbionts. Though these cases break our view of aphids harbouring a single obligate endosymbiont, we know little about the extent, nature, and evolution of these associations across aphid subfamilies. Here, using metagenomics on 25 aphid species from nine subfamilies, re-assembly and re-annotation of 20 aphid symbionts previously sequenced, and 16S rRNA amplicon sequencing on 223 aphid samples (147 species from 12 subfamilies), we show that dual symbioses have evolved anew at least six times. We also show that these secondary co-obligate symbionts have typically evolved from facultative symbiotic taxa. Genome-based metabolic inference confirms interdependencies between Buchnera and its partners for the production of essential nutrients but shows contributions vary across pairs of co-obligate associates. Fluorescent in situ hybridisation microscopy shows a common bacteriocyte localisation of two newly acquired symbionts. Lastly, patterns of Buchnera genome evolution reveal that small losses affecting a few key genes can be the onset of these dual systems, while large gene losses can occur without any co-obligate symbiont acquisition. Hence, the Buchnera-aphid association, often thought of as exclusive, seems more flexible, with a few metabolic losses having recurrently promoted the establishment of a new co-obligate symbiotic partner.
Type: Research article
CC-BY 4.0
@article{10_24072_pcjournal_278,
author = {Manzano-Mar{\'\i}n, Alejandro and Coeur d{\textquoteright}acier, Armelle and Clamens, Anne-Laure and Cruaud, Corinne and Barbe, Val\'erie and Jousselin, Emmanuelle},
title = {Co-obligate symbioses have repeatedly evolved across aphids, but partner identity and nutritional contributions vary across lineages},
journal = {Peer Community Journal},
eid = {e46},
publisher = {Peer Community In},
volume = {3},
year = {2023},
doi = {10.24072/pcjournal.278},
url = {https://peercommunityjournal.org/articles/10.24072/pcjournal.278/}
}
TY - JOUR AU - Manzano-Marín, Alejandro AU - Coeur d’acier, Armelle AU - Clamens, Anne-Laure AU - Cruaud, Corinne AU - Barbe, Valérie AU - Jousselin, Emmanuelle TI - Co-obligate symbioses have repeatedly evolved across aphids, but partner identity and nutritional contributions vary across lineages JO - Peer Community Journal PY - 2023 VL - 3 PB - Peer Community In UR - https://peercommunityjournal.org/articles/10.24072/pcjournal.278/ DO - 10.24072/pcjournal.278 ID - 10_24072_pcjournal_278 ER -
%0 Journal Article %A Manzano-Marín, Alejandro %A Coeur d’acier, Armelle %A Clamens, Anne-Laure %A Cruaud, Corinne %A Barbe, Valérie %A Jousselin, Emmanuelle %T Co-obligate symbioses have repeatedly evolved across aphids, but partner identity and nutritional contributions vary across lineages %J Peer Community Journal %D 2023 %V 3 %I Peer Community In %U https://peercommunityjournal.org/articles/10.24072/pcjournal.278/ %R 10.24072/pcjournal.278 %F 10_24072_pcjournal_278
Manzano-Marín, Alejandro; Coeur d’acier, Armelle; Clamens, Anne-Laure; Cruaud, Corinne; Barbe, Valérie; Jousselin, Emmanuelle. Co-obligate symbioses have repeatedly evolved across aphids, but partner identity and nutritional contributions vary across lineages. Peer Community Journal, Volume 3 (2023), article no. e46. doi : 10.24072/pcjournal.278. https://peercommunityjournal.org/articles/10.24072/pcjournal.278/
Peer reviewed and recommended by PCI : 10.24072/pci.evolbiol.100640
Conflict of interest of the recommender and peer reviewers:
The recommender in charge of the evaluation of the article and the reviewers declared that they have no conflict of interest (as defined in the code of conduct of PCI) with the authors or with the content of the article.
[1] Gapped BLAST and PSI-BLAST: a new generation of protein database search programs, Nucleic Acids Research, Volume 25 (1997) no. 17, pp. 3389-3402 | DOI
[2] SPAdes: A New Genome Assembly Algorithm and Its Applications to Single-Cell Sequencing, Journal of Computational Biology, Volume 19 (2012) no. 5, pp. 455-477 | DOI
[3] Lysine provisioning by horizontally acquired genes promotes mutual dependence between whitefly and two intracellular symbionts, PLOS Pathogens, Volume 17 (2021) no. 11 | DOI
[4] Biology of bacteriocyte-associated endosymbionts of plant sap-sucking insects, Annual Review of Microbiology, Volume 59 (2005) no. 1, pp. 155-189 | DOI
[5] Genetics, physiology, and evolutionary relationships of the genus Buchnera: Intracellular Symbionts of Aphids, Annual Review of Microbiology, Volume 49 (1995) no. 1, pp. 55-94 | DOI
[6] Small, Smaller, Smallest: The Origins and Evolution of Ancient Dual Symbioses in a Phloem-Feeding Insect, Genome Biology and Evolution, Volume 5 (2013) no. 9, pp. 1675-1688 | DOI
[7] Impact of Host Developmental Age on the Transcriptome of the Symbiotic Bacterium Buchnera aphidicola in the Pea Aphid ( Acyrthosiphon pisum ), Applied and Environmental Microbiology, Volume 75 (2009) no. 22, pp. 7294-7297 | DOI
[8] B-vitamin nutrition in the pea aphid-Buchnera symbiosis, Journal of Insect Physiology, Volume 126 (2020) | DOI
[9] Domain enhanced lookup time accelerated BLAST, Biology Direct, Volume 7 (2012) no. 1 | DOI
[10] Genomic erosion and extensive horizontal gene transfer in gut-associated Acetobacteraceae, BMC Genomics, Volume 20 (2019) no. 1 | DOI
[11] Endosymbiose der Tiere mit Pflanzlichen Mikroorganismen, Birkhäuser Basel, Basel, 1953 | DOI
[12] Massive Genomic Decay in Serratia symbiotica, a Recently Evolved Symbiont of Aphids, Genome Biology and Evolution, Volume 3 (2011), pp. 195-208 | DOI
[13] A dual endosymbiosis supports nutritional adaptation to hematophagy in the invasive tick Hyalomma marginatum, eLife, Volume 10 (2021) | DOI
[14] BLAST+: architecture and applications, BMC Bioinformatics, Volume 10 (2009) no. 1 | DOI
[15] CBGP - Continental arthropod collection. URL , 2018 | DOI
[16] tRNAscan-SE 2.0: improved detection and functional classification of transfer RNA genes, Nucleic Acids Research, Volume 49 (2021) no. 16, pp. 9077-9096 | DOI
[17] Fitness effects of two facultative endosymbiotic bacteria on the pea aphid, Acyrthosiphon pisum, and the blue alfalfa aphid, A. kondoi, Entomologia Experimentalis et Applicata, Volume 95 (2000) no. 3, pp. 315-323 | DOI
[18] Assessing Performance of Orthology Detection Strategies Applied to Eukaryotic Genomes, PLoS ONE, Volume 2 (2007) no. 4 | DOI
[19] Mitochondrial genome sequences effectively reveal deep branching events in aphids (Insecta: Hemiptera: Aphididae), Zoologica Scripta, Volume 46 (2017) no. 6, pp. 706-717 | DOI
[20] Occurrence and Transmission of Facultative Endosymbionts in Aphids, Current Microbiology, Volume 34 (1997) no. 4, pp. 220-225 | DOI
[21] Molecular phylogeny of Macrosiphini (Hemiptera: Aphididae): An evolutionary hypothesis for the Pterocomma-group habitat adaptation, Molecular Phylogenetics and Evolution, Volume 121 (2018), pp. 12-22 | DOI
[22] Evolutionary loss and replacement of Buchnera, the obligate endosymbiont of aphids, The ISME Journal, Volume 12 (2018) no. 3, pp. 898-908 | DOI
[23] Genome Evolution of the Obligate Endosymbiont Buchnera aphidicola, Molecular Biology and Evolution, Volume 36 (2019) no. 7, pp. 1481-1489 | DOI
[24] Proposed minimal standards for the use of genome data for the taxonomy of prokaryotes, International Journal of Systematic and Evolutionary Microbiology, Volume 68 (2018) no. 1, pp. 461-466 | DOI
[25] Ribosomal Database Project: data and tools for high throughput rRNA analysis, Nucleic Acids Research, Volume 42 (2014) no. D1 | DOI
[26] Long-Term Evolutionary Stability of Bacterial Endosymbiosis in Curculionoidea: Additional Evidence of Symbiont Replacement in the Dryophthoridae Family, Molecular Biology and Evolution, Volume 25 (2008) no. 5, pp. 859-868 | DOI
[27] Count: evolutionary analysis of phylogenetic profiles with parsimony and likelihood, Bioinformatics, Volume 26 (2010) no. 15, pp. 1910-1912 | DOI
[28] jModelTest 2: more models, new heuristics and parallel computing, Nature Methods, Volume 9 (2012) no. 8, p. 772-772 | DOI
[29] Transitional genomes and nutritional role reversals identified for dual symbionts of adelgids (Aphidoidea: Adelgidae), The ISME Journal, Volume 16 (2022) no. 3, pp. 642-654 | DOI
[30] A test of morphological hypotheses for tribal and subtribal relationships of Aphidinae (Insecta: Hemiptera: Aphididae) using DNA sequences, Molecular Phylogenetics and Evolution, Volume 38 (2006) no. 2, pp. 316-329 | DOI
[31] Diversity of proteobacterial endosymbionts in hemlock woolly adelgid (Adelges tsugae) (Hemiptera: Adelgidae) from its native and introduced range, Environmental Microbiology, Volume 15 (2013) no. 7, pp. 2043-2062 | DOI
[32] Molecular data support a rapid radiation of aphids in the Cretaceous and multiple origins of host alternation, Biological Journal of the Linnean Society, Volume 71 (2000) no. 4, pp. 689-717 | DOI
[33] Dynamic Acquisition and Loss of Dual-Obligate Symbionts in the Plant-Sap-Feeding Adelgidae (Hemiptera: Sternorrhyncha: Aphidoidea), Frontiers in Microbiology, Volume 8 (2017) | DOI
[34] Protection of Pea Aphids Associated with Coinfecting Bacterial Symbionts Persists During Superparasitism by a Braconid Wasp, Microbial Ecology, Volume 71 (2016) no. 1, pp. 1-4 | DOI
[35] Aphid Heritable Symbiont Exploits Defensive Mutualism, Applied and Environmental Microbiology, Volume 83 (2017) no. 8 | DOI
[36] Nutritional Interactions in Insect-Microbial Symbioses: Aphids and Their Symbiotic Bacteria Buchnera, Annual Review of Entomology, Volume 43 (1998) no. 1, pp. 17-37 | DOI
[37] Phloem-sap feeding by animals: problems and solutions, Journal of Experimental Botany, Volume 57 (2006) no. 4, pp. 747-754 | DOI
[38] Evolution ofWolbachiamutualism and reproductive parasitism: insight from two novel strains that co-infect cat fleas, PeerJ, Volume 8 (2020) | DOI
[39] Tick-Bacteria Mutualism Depends on B Vitamin Synthesis Pathways, Current Biology, Volume 28 (2018) no. 12 | DOI
[40] MUSCLE: multiple sequence alignment with high accuracy and high throughput, Nucleic Acids Research, Volume 32 (2004) no. 5, pp. 1792-1797 | DOI
[41] FROGS: Find, Rapidly, OTUs with Galaxy Solution, Bioinformatics, Volume 34 (2017) no. 8, pp. 1287-1294 | DOI
[42] Aphid Species File. Version 5.0/5.0, 2022 (http://aphid.speciesfile.org)
[43] leBIBIQBPP: a set of databases and a webtool for automatic phylogenetic analysis of prokaryotic sequences, BMC Bioinformatics, Volume 16 (2015) no. 1 | DOI
[44] Secondary Intracellular Symbiotic Bacteria in Aphids of the GenusYamatocallis(Homoptera: Aphididae: Drepanosiphinae), Applied and Environmental Microbiology, Volume 67 (2001) no. 11, pp. 5315-5320 | DOI
[45] A novel eukaryotic extracellular symbiont in an aphid, Astegopteryx styraci (Homoptera, Aphididae, Hormaphidinae), Journal of Insect Physiology, Volume 38 (1992) no. 10, pp. 765-773 | DOI
[46] Occurrence of Chaperonin 60 and Chaperonin 10 in primary and secondary bacterial symbionts of aphids: Implications for the evolution of an endosymbiotic system in aphids, Journal of Molecular Evolution, Volume 36 (1993) no. 6, pp. 568-577 | DOI
[47] Phylogeny of Cerataphidini aphids revealed by their symbiotic microorganisms and basic structure of their galls - Implications for host-symbiont coevolution and evolution of sterile soldier castes, Zoological Science, Volume 11 (1994)
[48] The Secondary Endosymbiotic Bacterium of the Pea AphidAcyrthosiphon pisum(Insecta: Homoptera), Applied and Environmental Microbiology, Volume 66 (2000) no. 7, pp. 2748-2758 | DOI
[49] Intraspecific phylogenetic congruence among multiple symbiont genomes, Proceedings of the Royal Society of London. Series B: Biological Sciences, Volume 267 (2000) no. 1461, pp. 2517-2521 | DOI
[50] Comparative genomics provides a timeframe for Wolbachia evolution and exposes a recent biotin synthesis operon transfer, Nature Microbiology, Volume 2 (2017) no. 3 | DOI
[51] Plasmids in the aphid endosymbiont Buchnera aphidicola with the smallest genomes. A puzzling evolutionary story, Gene, Volume 370 (2006), pp. 17-25 | DOI
[52] Aphid genome expression reveals host–symbiont cooperation in the production of amino acids, Proceedings of the National Academy of Sciences, Volume 108 (2011) no. 7, pp. 2849-2854 | DOI
[53] A facultative endosymbiont in aphids can provide diverse ecological benefits, Journal of Evolutionary Biology, Volume 28 (2015) no. 10, pp. 1753-1760 | DOI
[54] The fine structure of the mycetome symbiotes of the aphids Brevicoryne brassicae, Myzus persicae, and Macrosiphum rosae, Journal of Insect Physiology, Volume 17 (1971) no. 10, pp. 2035-2050 | DOI
[55] Carpenter Bees (Xylocopa) harbor a distinctive gut microbiome related to that of honey bees and bumble bees, Applied and Environmental Microbiology, Volume 88 (2022) no. 13 | DOI
[56] Obligate bacterial mutualists evolving from environmental bacteria in natural insect populations, Nature Microbiology, Volume 1 (2016) no. 1 | DOI
[57] Repeated replacement of an intrabacterial symbiont in the tripartite nested mealybug symbiosis, Proceedings of the National Academy of Sciences, Volume 113 (2016) no. 37 | DOI
[58] Multiple origins of endosymbiosis within the Enterobacteriaceae (γ-Proteobacteria): convergence of complex phylogenetic approaches, BMC Biology, Volume 9 (2011) no. 1 | DOI
[59] Horizontal Gene Transfer from Diverse Bacteria to an Insect Genome Enables a Tripartite Nested Mealybug Symbiosis, Cell, Volume 153 (2013) no. 7, pp. 1567-1578 | DOI
[60] Fine-scale cospeciation between Brachycaudus and Buchnera aphidicola: bacterial genome helps define species and evolutionary relationships in aphids, Proceedings of the Royal Society B: Biological Sciences, Volume 276 (2009) no. 1654, pp. 187-196 | DOI
[61] Assessment of a 16S rRNA amplicon Illumina sequencing procedure for studying the microbiome of a symbiont-rich aphid genus, Molecular Ecology Resources, Volume 16 (2016) no. 3, pp. 628-640 | DOI
[62] Rfam 14: expanded coverage of metagenomic, viral and microRNA families, Nucleic Acids Research, Volume 49 (2021) no. D1 | DOI
[63] MAFFT Multiple Sequence Alignment Software Version 7: Improvements in Performance and Usability, Molecular Biology and Evolution, Volume 30 (2013) no. 4, pp. 772-780 | DOI
[64] Macroevolutionary Patterns in the Aphidini Aphids (Hemiptera: Aphididae): Diversification, Host Association, and Biogeographic Origins, PLoS ONE, Volume 6 (2011) no. 9 | DOI
[65] Swapping symbionts in spittlebugs: evolutionary replacement of a reduced genome symbiont, The ISME Journal, Volume 8 (2014) no. 6, pp. 1237-1246 | DOI
[66] Changing partners in an obligate symbiosis: a facultative endosymbiont can compensate for loss of the essential endosymbiontBuchnerain an aphid, Proceedings of the Royal Society of London. Series B: Biological Sciences, Volume 270 (2003) no. 1533, pp. 2543-2550 | DOI
[67] Quenching autofluorescence of insect tissues for in situ detection of endosymbionts, Applied Entomology and Zoology, Volume 44 (2009) no. 2, pp. 281-291 | DOI
[68] Ovariole structure in viviparous and oviparous generations of Glyphina betulae (Linnaeus 1758) (Insecta, Hemiptera, Aphidinea: Thelaxidae). , Aphids and Other Hemipterous Insects, Volume 18 (2012) (https://www.kul.pl/files/658/aphids18/02_Kot.pdf)
[69] Development of a Dual-Index Sequencing Strategy and Curation Pipeline for Analyzing Amplicon Sequence Data on the MiSeq Illumina Sequencing Platform, Applied and Environmental Microbiology, Volume 79 (2013) no. 17, pp. 5112-5120 | DOI
[70] Cultivation and characterization of the gut symbionts of honey bees and bumble bees: description of Snodgrassella alvi gen. nov., sp. nov., a member of the family Neisseriaceae of the Betaproteobacteria , and Gilliamella apicola gen. nov., sp. nov., a member of Orbaceae fam. nov., Orbales ord. nov., a sister taxon to the order ‘ Enterobacteriales ’ of the Gammaproteobacteria, International Journal of Systematic and Evolutionary Microbiology, Volume 63 (2013) no. Pt_6, pp. 2008-2018 | DOI
[71] Evolution of the secondary symbiont “Candidatus Serratia symbiotica” in aphid species of the subfamily Lachninae, Applied and Environmental Microbiology, Volume 74 (2008) no. 13, pp. 4236-4240 | DOI
[72] New Clues about the Evolutionary History of Metabolic Losses in Bacterial Endosymbionts, Provided by the Genome of Buchnera aphidicola from the Aphid Cinara tujafilina, Applied and Environmental Microbiology, Volume 77 (2011) no. 13, pp. 4446-4454 | DOI
[73] Serratia symbiotica from the Aphid Cinara cedri: A Missing Link from Facultative to Obligate Insect Endosymbiont, PLoS Genetics, Volume 7 (2011) no. 11 | DOI
[74] ARAGORN, a program to detect tRNA genes and tmRNA genes in nucleotide sequences, Nucleic Acids Research, Volume 32 (2004) no. 1, pp. 11-16 | DOI
[75] Endosymbiont Phylogenesis in the Dryophthoridae Weevils: Evidence for Bacterial Replacement, Molecular Biology and Evolution, Volume 21 (2004) no. 6, pp. 965-973 | DOI
[76] OrthoMCL: Identification of Ortholog Groups for Eukaryotic Genomes, Genome Research, Volume 13 (2003) no. 9, pp. 2178-2189 | DOI
[77] Is the subfamily Eriosomatinae (Hemiptera: Aphididae) monophyletic? , Turkish Journal of Zoology (2014) no. 38
[78] Metabolic Coevolution in the Bacterial Symbiosis of Whiteflies and Related Plant Sap-Feeding Insects, Genome Biology and Evolution, Volume 7 (2015) no. 9, pp. 2635-2647 | DOI
[79] Multiple origins of interdependent endosymbiotic complexes in a genus of cicadas, Proceedings of the National Academy of Sciences, Volume 115 (2018) no. 2 | DOI
[80] FLASH: fast length adjustment of short reads to improve genome assemblies, Bioinformatics, Volume 27 (2011) no. 21, pp. 2957-2963 | DOI
[81] Swarm: robust and fast clustering method for amplicon-based studies, PeerJ, Volume 2 (2014) | DOI
[82] No evidence for Wolbachia as a nutritional co-obligate endosymbiont in the aphid Pentalonia nigronervosa, Microbiome, Volume 8 (2020) no. 1 | DOI
[83] 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 Biology and Evolution, Volume 6 (2014) no. 7, pp. 1683-1698 | DOI
[84] Snapshots of a shrinking partner: Genome reduction in Serratia symbiotica, Scientific Reports, Volume 6 (2016) no. 1 | DOI
[85] Reinventing the Wheel and Making It Round Again: Evolutionary Convergence inBuchnera–SerratiaSymbiotic Consortia between the Distantly Related Lachninae AphidsTuberolachnus salignusandCinara cedri, Genome Biology and Evolution, Volume 8 (2014) no. 5, pp. 1440-1458 | DOI
[86] Happens in the best of subfamilies: establishment and repeated replacements of co‐obligate secondary endosymbionts within Lachninae aphids, Environmental Microbiology, Volume 19 (2017) no. 1, pp. 393-408 | DOI
[87] A Freeloader? The Highly Eroded Yet Large Genome of the Serratia symbiotica Symbiont of Cinara strobi, Genome Biology and Evolution, Volume 10 (2018) no. 9, pp. 2178-2189 | DOI
[88] Serial horizontal transfer of vitamin-biosynthetic genes enables the establishment of new nutritional symbionts in aphids’ di-symbiotic systems, The ISME Journal, Volume 14 (2020) no. 1, pp. 259-273 | DOI
[89] Post-publication review of Monnin et. al. (2020), ”Parallel evolution in the integration of a co-obligate aphid symbiosis”, PubPeer, 2020 (https://pubpeer.com/publications/51CF51BF8B00F33721655DB14425F4)
[90] Cutadapt removes adapter sequences from high-throughput sequencing reads, EMBnet.journal, Volume 17 (2011) no. 1 | DOI
[91] Recurrent symbiont recruitment from fungal parasites in cicadas, Proceedings of the National Academy of Sciences, Volume 115 (2018) no. 26 | DOI
[92] Parallel genomic evolution and metabolic interdependence in an ancient symbiosis, Proceedings of the National Academy of Sciences, Volume 104 (2007) no. 49, pp. 19392-19397 | DOI
[93] An Interdependent Metabolic Patchwork in the Nested Symbiosis of Mealybugs, Current Biology, Volume 21 (2011) no. 16, pp. 1366-1372 | DOI
[94] The Life of an Insect Endosymbiont from the Cradle to the Grave, Current Biology, Volume 29 (2019) no. 11 | DOI
[95] Buchnerahas changed flatmate but the repeated replacement of co-obligate symbionts is not associated with the ecological expansions of their aphid hosts, Molecular Ecology, Volume 26 (2017) no. 8, pp. 2363-2378 | DOI
[96] Ovary structure and transovarial transmission of endosymbiotic microorganisms in Clethrobius comes, Myzocallis walshii and Sipha maydis /Hemiptera, Aphididae: Drepanosiphinae., Aphids and Other Hemipterous Insects , Volume 16 (2010)
[97] Endosymbiotic microorganisms of aphids (Hemiptera: Sternorrhyncha: Aphidoidea): Ultrastructure, distribution and transovarial transmission, European Journal of Entomology, Volume 111 (2014) no. 1, pp. 91-104 | DOI
[98] Alternative Transmission Patterns in Independently Acquired Nutritional Cosymbionts of Dictyopharidae Planthoppers, mBio, Volume 12 (2021) no. 4 | DOI
[99] Taxonomic Classification of Bacterial 16S rRNA Genes Using Short Sequencing Reads: Evaluation of Effective Study Designs, PLoS ONE, Volume 8 (2013) no. 1 | DOI
[100] Parallel Evolution in the Integration of a Co-obligate Aphid Symbiosis, Current Biology, Volume 30 (2020) no. 10 | DOI
[101] Facultative bacterial endosymbionts benefit pea aphidsAcyrthosiphon pisumunder heat stress, Ecological Entomology, Volume 27 (2002) no. 2, pp. 189-195 | DOI
[102] A molecular clock in endosymbiotic bacteria is calibrated using the insect hosts, Proceedings of the Royal Society of London. Series B: Biological Sciences, Volume 253 (1993) no. 1337, pp. 167-171 | DOI
[103] Evolutionary Relationships of Three New Species of Enterobacteriaceae Living as Symbionts of Aphids and Other Insects, Applied and Environmental Microbiology, Volume 71 (2005) no. 6, pp. 3302-3310 | DOI
[104] Defensive Bacteriome Symbiont with a Drastically Reduced Genome, Current Biology, Volume 23 (2013) no. 15, pp. 1478-1484 | DOI
[105] Comparative Genomics Underlines Multiple Roles of Profftella, an Obligate Symbiont of Psyllids: Providing Toxins, Vitamins, and Carotenoids, Genome Biology and Evolution, Volume 12 (2020) no. 11, pp. 1975-1987 | DOI
[106] Structural RNA homology search and alignment using covariance models, PhD thesis, Washington University in Saint Louis (2009) (http://eddylab.org/publications/Nawrocki09b/Nawrocki09b-phdthesis.pdf)
[107] Infernal 1.1: 100-fold faster RNA homology searches, Bioinformatics, Volume 29 (2013) no. 22, pp. 2933-2935 | DOI
[108] Evolutionary origin of insect–Wolbachia nutritional mutualism, Proceedings of the National Academy of Sciences, Volume 111 (2014) no. 28, pp. 10257-10262 | DOI
[109] Genome sequence of “Candidatus Serratia symbiotica” strain IS, a facultative bacterial symbiont of the pea aphid Acyrthosiphon pisum, Microbiology Resource Announcements, Volume 8 (2019) no. 19 | DOI
[110] Reconstructing the phylogeny of aphids (Hemiptera: Aphididae) using DNA of the obligate symbiont Buchnera aphidicola, Molecular Phylogenetics and Evolution, Volume 68 (2013) no. 1, pp. 42-54 | DOI
[111] Unipro UGENE: a unified bioinformatics toolkit, Bioinformatics, Volume 28 (2012) no. 8, pp. 1166-1167 | DOI
[112] Facultative bacterial symbionts in aphids confer resistance to parasitic wasps, Proceedings of the National Academy of Sciences, Volume 100 (2003) no. 4, pp. 1803-1807 | DOI
[113] Combination of molecular data support the existence of three main lineages in the phylogeny of aphids (Hemiptera: Aphididae) and the basal position of the subfamily Lachninae, Molecular Phylogenetics and Evolution, Volume 55 (2010) no. 1, pp. 305-317 | DOI
[114] Drosophila melanogaster establishes a species-specific mutualistic interaction with stable gut-colonizing bacteria, PLOS Biology, Volume 16 (2018) no. 7 | DOI
[115] Cultivation-assisted genome of Candidatus Fukatsuia symbiotica; the enigmatic ‘X-type’ symbiont of aphids, Genome Biology and Evolution (2019) | DOI
[116] The invertible P-DNA segment in the chromosome of Escherichia coli., The EMBO Journal, Volume 4 (1985) no. 1, pp. 237-242 | DOI
[117] Circulation of the Cultivable Symbiont Serratia symbiotica in Aphids Is Mediated by Plants, Frontiers in Microbiology, Volume 10 (2019) | DOI
[118] Pervasiveness of the symbiont Serratia symbiotica in the aphid natural environment: distribution, diversity and evolution at a multitrophic level, FEMS Microbiology Ecology, Volume 98 (2022) no. 1 | DOI
[119] The SILVA ribosomal RNA gene database project: improved data processing and web-based tools, Nucleic Acids Research, Volume 41 (2013) no. D1 | DOI
[120] Biotin provisioning by horizontally transferred genes from bacteria confers animal fitness benefits, The ISME Journal, Volume 14 (2020) no. 10, pp. 2542-2553 | DOI
[121] Compartmentalized into Bacteriocytes but Highly Invasive: the Puzzling Case of the Co-Obligate Symbiont Serratia symbiotica in the Aphid Periphyllus lyropictus, Microbiology Spectrum, Volume 10 (2022) no. 3 | DOI
[122] A new symbiotic lineage related to Neisseria and Snodgrassella arises from the dynamic and diverse microbiomes in sucking lice, Molecular Ecology, Volume 30 (2021) no. 9, pp. 2178-2196 | DOI
[123] Legionella becoming a mutualist: Adaptive processes shaping the genome of symbiont in the mouse Polyplax serrata, Genome Biology and Evolution, Volume 9 (2017) no. 11, pp. 2946-2957 | DOI
[124] VSEARCH: a versatile open source tool for metagenomics, PeerJ, Volume 4 (2016) | DOI
[125] MrBayes 3.2: Efficient Bayesian Phylogenetic Inference and Model Choice Across a Large Model Space, Systematic Biology, Volume 61 (2012) no. 3, pp. 539-542 | DOI
[126] The Protector within: Comparative Genomics of APSE Phages across Aphids Reveals Rampant Recombination and Diverse Toxin Arsenals, Genome Biology and Evolution, Volume 12 (2020) no. 6, pp. 878-889 | DOI
[127] Costs and benefits of symbiont infection in aphids: variation among symbionts and across temperatures, Proceedings of the Royal Society B: Biological Sciences, Volume 273 (2006) no. 1586, pp. 603-610 | DOI
[128] How nutritionally imbalanced is phloem sap for aphids?, Entomologia Experimentalis et Applicata, Volume 91 (1999) no. 1, pp. 203-210 | DOI
[129] The All-Rounder Sodalis: A New Bacteriome-Associated Endosymbiont of the Lygaeoid Bug Henestaris halophilus (Heteroptera: Henestarinae) and a Critical Examination of Its Evolution, Genome Biology and Evolution, Volume 9 (2017) no. 10, pp. 2893-2910 | DOI
[130] Quality control and preprocessing of metagenomic datasets, Bioinformatics, Volume 27 (2011) no. 6, pp. 863-864 | DOI
[131] Prokka: rapid prokaryotic genome annotation, Bioinformatics, Volume 30 (2014) no. 14, pp. 2068-2069 | DOI
[132] Genome sequence of the endocellular bacterial symbiont of aphids Buchnera sp. APS, Nature, Volume 407 (2000) no. 6800, pp. 81-86 | DOI
[133] Genome Reduction and Co-evolution between the Primary and Secondary Bacterial Symbionts of Psyllids, Molecular Biology and Evolution, Volume 29 (2012) no. 12, pp. 3781-3792 | DOI
[134] Parallel Histories of Horizontal Gene Transfer Facilitated Extreme Reduction of Endosymbiont Genomes in Sap-Feeding Insects, Molecular Biology and Evolution, Volume 31 (2014) no. 4, pp. 857-871 | DOI
[135] Genomic Signatures of Honey Bee Association in an Acetic Acid Symbiont, Genome Biology and Evolution, Volume 12 (2020) no. 10, pp. 1882-1894 | DOI
[136] Deciphering host-parasitoid interactions and parasitism rates of crop pests using DNA metabarcoding, Scientific Reports, Volume 9 (2019) no. 1 | DOI
[137] Symbiont Acquisition and Replacement as a Source of Ecological Innovation, Trends in Microbiology, Volume 25 (2017) no. 5, pp. 375-390 | DOI
[138] Convergent patterns in the evolution of mealybug symbioses involving different intrabacterial symbionts, The ISME Journal, Volume 11 (2017) no. 3, pp. 715-726 | DOI
[139] Evolutionarily recent dual obligatory symbiosis among adelgids indicates a transition between fungus- and insect-associated lifestyles, The ISME Journal, Volume 16 (2022) no. 1, pp. 247-256 | DOI
[140] Transovarial Transmission of Symbionts in Insects, Results and Problems in Cell Differentiation, Springer International Publishing, Cham, 2017, pp. 43-67 | DOI
[141] Improvement of Phylogenies after Removing Divergent and Ambiguously Aligned Blocks from Protein Sequence Alignments, Systematic Biology, Volume 56 (2007) no. 4, pp. 564-577 | DOI
[142] Endosymbiont gene functions impaired and rescued by polymerase infidelity at poly(A) tracts, Proceedings of the National Academy of Sciences, Volume 105 (2008) no. 39, pp. 14934-14939 | DOI
[143] Co-evolution and symbiont replacement shaped the symbiosis between adelgids (Hemiptera: Adelgidae) and their bacterial symbionts, Environmental Microbiology, Volume 14 (2012) no. 5, pp. 1284-1295 | DOI
[144] The Pine Bark Adelgid, Pineus strobi, Contains Two Novel Bacteriocyte-Associated Gammaproteobacterial Symbionts, Applied and Environmental Microbiology, Volume 80 (2014) no. 3, pp. 878-885 | DOI
[145] Diversification of endosymbiosis: replacements, co-speciation and promiscuity of bacteriocyte symbionts in weevils, The ISME Journal, Volume 7 (2013) no. 7, pp. 1378-1390 | DOI
[146] Melanaphis sacchari strain: LSU and endosymbiont genome sequencing and assembly. National Center for Biotechnology Information. dataset, 2022 (https://data.nal.usda.gov/dataset/melanaphis-sacchari-strainlsu-and-endosymbiont-genome-sequencing-and-assembly)
[147] Putative evolutionary origin of plasmids carrying the genes involved in leucine biosynthesis in Buchnera aphidicola (endosymbiont of aphids), Journal of Bacteriology, Volume 179 (1997) no. 15, pp. 4768-4777 | DOI
[148] Postsymbiotic plasmid acquisition and evolution of the repA1 -replicon in Buchnera aphidicola, Proceedings of the National Academy of Sciences, Volume 97 (2000) no. 20, pp. 10855-10860 | DOI
[149] Reductive genome evolution in Buchnera aphidicola, Proceedings of the National Academy of Sciences, Volume 100 (2003) no. 2, pp. 581-586 | DOI
[150] Functional and Evolutionary Analysis of the Genome of an Obligate Fungal Symbiont, Genome Biology and Evolution, Volume 5 (2013) no. 5, pp. 891-904 | DOI
[151] Molecular data support a rapid radiation of aphids in the Cretaceous and multiple origins of host alternation, Biological Journal of the Linnean Society, Volume 71 (2000) no. 4, pp. 689-717 | DOI
[152] Diversity of proteobacterial endosymbionts in hemlock woolly adelgid (Adelges tsugae) (Hemiptera: Adelgidae) from its native and introduced range, Environmental Microbiology, Volume 15 (2013) no. 7, pp. 2043-2062 | DOI
[153] Horizontal Gene Transfer to a Defensive Symbiont with a Reduced Genome in a Multipartite Beetle Microbiome, mBio, Volume 11 (2020) no. 1 | DOI
[154] Partnering With a Pest: Genomes of Hemlock Woolly Adelgid Symbionts Reveal Atypical Nutritional Provisioning Patterns in Dual-Obligate Bacteria, Genome Biology and Evolution, Volume 10 (2018) no. 6, pp. 1607-1621 | DOI
[155] Slip into Something More Functional: Selection Maintains Ancient Frameshifts in Homopolymeric Sequences, Molecular Biology and Evolution, Volume 27 (2010) no. 4, pp. 833-839 | DOI
[156] The invasive MED/Q Bemisia tabaci genome: a tale of gene loss and gene gain, BMC Genomics, Volume 19 (2018) no. 1 | DOI
[157] Uniting the classification of cultured and uncultured bacteria and archaea using 16S rRNA gene sequences, Nature Reviews Microbiology, Volume 12 (2014) no. 9, pp. 635-645 | DOI
[158] Complex host/symbiont integration of a multi-partner symbiotic system in the eusocial aphid Ceratovacuna japonica, iScience, Volume 25 (2022) no. 12 | DOI
[159] Nature of Transported Substances, Transport in Plants I, Springer Berlin Heidelberg, Berlin, Heidelberg, 1975, pp. 59-100 | DOI
[160] The natural occurrence of secondary bacterial symbionts in aphids, Ecological Entomology, Volume 41 (2016) no. 1, pp. 13-26 | DOI
Cited by Sources: