publication . Conference object . Article . 2018

Multi-scale characterization of symbiont diversity in the pea aphid complex through metagenomic approaches

Guyomar, Cervin; Legeai, Fabrice; Jousselin, Emmanuelle; Mougel, Christophe,; Lemaitre, Claire; Simon, Jean-Christophe;
Open Access English
  • Published: 01 Dec 2018
  • Publisher: HAL CCSD
Abstract
Background Most metazoans are involved in durable relationships with microbes which can take several forms, from mutualism to parasitism. The advances of NGS technologies and bioinformatics tools have opened opportunities to shed light on the diversity of microbial communities and to give some insights into the functions they perform in a broad array of hosts. The pea aphid is a model system for the study of insect-bacteria symbiosis. It is organized in a complex of biotypes, each adapted to specific host plants. It harbors both an obligatory symbiont supplying key nutrients and several facultative symbionts bringing additional functions to the host, such as pro...
Subjects
Medical Subject Headings: food and beveragesbiochemical phenomena, metabolism, and nutrition
free text keywords: [SDV.BIBS]Life Sciences [q-bio]/Quantitative Methods [q-bio.QM], Host-microbiota interactions;Aphids;Metagenomics;Symbiosis;Phylogeny, Symbiosis, Phylogeny, Metagenomics, Host-microbiota interactions, Aphids, [INFO.INFO-BI]Computer Science [cs]/Bioinformatics [q-bio.QM], Research, QR100-130, Holobiont, Phylogenetics, Evolutionary biology, Microbial ecology, Facultative, Biology, Mutualism (biology), Aphid, biology.organism_classification, Evolutionary dynamics
93 references, page 1 of 7

1. Munson MA, Baumann P, Clark MA, Baumann L, Moran NA, Voegtlin DJ, et al. Evidence for the establishment of aphid-eubacterium endosymbiosis in an ancestor of four aphid families. J Bacteriol. 1991;173:6321-4 American Society for Microbiology. Available from: http://www.ncbi.nlm.nih.gov/ pubmed/1917864. Cited 26 Oct 2017.

2. Thao ML, Moran NA, Abbot P, Brennan EB, Burckhardt DH, Baumann P. Cospeciation of psyllids and their primary prokaryotic endosymbionts. Appl Environ Microbiol. 2000;66:2898-905 American Society for Microbiology. Available from: http://www.ncbi.nlm.nih.gov/pubmed/10877784. Cited 26 Oct 2017.

3. Gil R, Sabater-Muñoz B, Latorre A, Silva FJ, Moya A. Extreme genome reduction in Buchnera spp.: toward the minimal genome needed for symbiotic life. Proc Natl Acad Sci U S A. 2002;99:4454-8 National Academy of Sciences. Available from: http://www.pnas.org/content/99/7/4454. abstract?ijkey=69c46a4045e4960a41f9952c500b9364a3f744e8&keytype2=tf_ ipsecsha. Cited 15 Oct 2017.

4. Charlat S, Hurst GDD, Merçot H. Evolutionary consequences of Wolbachia infections. Trends Genet. 2003;19:217-23 Elsevier Current Trends. Available from: http://www.sciencedirect.com/science/article/pii/S0168952503000246. Cited 15 Oct 2017. [OpenAIRE]

5. Oliver KM, Russell JA, Moran NA, Hunter MS. Facultative bacterial symbionts in aphids confer resistance to parasitic wasps. Proc Natl Acad Sci. 2003;100: 1803-7 National Academy of Sciences. Available from: http://www.pnas.org/ cgi/doi/10.1073/pnas.0335320100. Cited 17 Oct 2017.

6. Russell JA, Moran NA. Costs and benefits of symbiont infection in aphids: variation among symbionts and across temperatures. Proc Biol Sci. 2006;273: 603-10 Available from: http://www.ncbi.nlm.nih.gov/pubmed/ 16537132%5Cn http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid= PMC1560055%5Cn http://rspb.royalsocietypublishing.org.gate1.inist.fr/ content/273/1586/603.short. Cited 17 Oct 2017.

7. Christian N, Whitaker BK, Clay K. Microbiomes: unifying animal and plant systems through the lens of community ecology theory. Front Microbiol. 2015;6:869 Frontiers. Available from: http://journal.frontiersin.org/Article/10. 3389/fmicb.2015.00869/abstract. Cited 18 Apr 2018.

8. McFall-Ngai M, Hadfield MG, Bosch TCG, Carey HV, Domazet-Lošo T, Douglas AE, et al. Animals in a bacterial world, a new imperative for the life sciences. Proc Natl Acad Sci. 2013;110:3229-36 National Academy of Sciences. Available from: http://www.pnas.org/lookup/doi/10.1073/pnas. 1218525110. Cited 18 Apr 2018.

9. Rosenberg E, Koren O, Reshef L, Efrony R, Zilber-Rosenberg I. The role of microorganisms in coral health, disease and evolution. Nat Rev Microbiol. 2007;5:355-62 Available from: http://www.nature.com/doifinder/10.1038/ nrmicro1635.

10. Rohwer F, Seguritan V, Azam F, Knowlton N. Diversity and distribution of coral-associated bacteria. Mar Ecol Prog Ser. 2002;243:1-10.

11. Bordenstein SR, Theis KR. Host biology in light of the microbiome: ten principles of holobionts and hologenomes. PLoS Biol. 2015;13:e1002226 Waldor MK, editor. Cambridge University Press. Available from: http://dx. plos.org/10.1371/journal.pbio.1002226. Cited 15 Oct 2017. [OpenAIRE]

12. Douglas AE, Werren JH. Holes in the hologenome: why host-microbe symbioses are not holobionts. MBio. 2016;7:e02099 American Society for Microbiology. Available from: http://www.ncbi.nlm.nih.gov/pubmed/ 27034285. Cited 5 Oct 2017.

13. Douglas AE. How multi-partner endosymbioses function. Nat Rev Microbiol. 2016;14:731-43 Available from: http://www.nature.com/doifinder/10.1038/ nrmicro.2016.151. Cited 15 Nov 2017.

14. Jaspers E, Overmann J. Ecological significance of microdiversity: identical 16S rRNA gene sequences can be found in bacteria with highly divergent genomes and ecophysiologies. Appl Environ Microbiol. 2004;70:4831-9 American Society for Microbiology. Available from: http://www.ncbi.nlm.nih. gov/pubmed/15294821. Cited 5 Oct 2017.

15. Thomas GH, Zucker J, Macdonald SJ, Sorokin A, Goryanin I, Douglas AE. A fragile metabolic network adapted for cooperation in the symbiotic bacterium Buchnera aphidicola. BMC Syst Biol. 2009;3:24 BioMed Central. Available from: http://bmcsystbiol.biomedcentral.com/articles/10.1186/1752- 0509-3-24. Cited 17 Nov 2017.

93 references, page 1 of 7
Abstract
Background Most metazoans are involved in durable relationships with microbes which can take several forms, from mutualism to parasitism. The advances of NGS technologies and bioinformatics tools have opened opportunities to shed light on the diversity of microbial communities and to give some insights into the functions they perform in a broad array of hosts. The pea aphid is a model system for the study of insect-bacteria symbiosis. It is organized in a complex of biotypes, each adapted to specific host plants. It harbors both an obligatory symbiont supplying key nutrients and several facultative symbionts bringing additional functions to the host, such as pro...
Subjects
Medical Subject Headings: food and beveragesbiochemical phenomena, metabolism, and nutrition
free text keywords: [SDV.BIBS]Life Sciences [q-bio]/Quantitative Methods [q-bio.QM], Host-microbiota interactions;Aphids;Metagenomics;Symbiosis;Phylogeny, Symbiosis, Phylogeny, Metagenomics, Host-microbiota interactions, Aphids, [INFO.INFO-BI]Computer Science [cs]/Bioinformatics [q-bio.QM], Research, QR100-130, Holobiont, Phylogenetics, Evolutionary biology, Microbial ecology, Facultative, Biology, Mutualism (biology), Aphid, biology.organism_classification, Evolutionary dynamics
93 references, page 1 of 7

1. Munson MA, Baumann P, Clark MA, Baumann L, Moran NA, Voegtlin DJ, et al. Evidence for the establishment of aphid-eubacterium endosymbiosis in an ancestor of four aphid families. J Bacteriol. 1991;173:6321-4 American Society for Microbiology. Available from: http://www.ncbi.nlm.nih.gov/ pubmed/1917864. Cited 26 Oct 2017.

2. Thao ML, Moran NA, Abbot P, Brennan EB, Burckhardt DH, Baumann P. Cospeciation of psyllids and their primary prokaryotic endosymbionts. Appl Environ Microbiol. 2000;66:2898-905 American Society for Microbiology. Available from: http://www.ncbi.nlm.nih.gov/pubmed/10877784. Cited 26 Oct 2017.

3. Gil R, Sabater-Muñoz B, Latorre A, Silva FJ, Moya A. Extreme genome reduction in Buchnera spp.: toward the minimal genome needed for symbiotic life. Proc Natl Acad Sci U S A. 2002;99:4454-8 National Academy of Sciences. Available from: http://www.pnas.org/content/99/7/4454. abstract?ijkey=69c46a4045e4960a41f9952c500b9364a3f744e8&keytype2=tf_ ipsecsha. Cited 15 Oct 2017.

4. Charlat S, Hurst GDD, Merçot H. Evolutionary consequences of Wolbachia infections. Trends Genet. 2003;19:217-23 Elsevier Current Trends. Available from: http://www.sciencedirect.com/science/article/pii/S0168952503000246. Cited 15 Oct 2017. [OpenAIRE]

5. Oliver KM, Russell JA, Moran NA, Hunter MS. Facultative bacterial symbionts in aphids confer resistance to parasitic wasps. Proc Natl Acad Sci. 2003;100: 1803-7 National Academy of Sciences. Available from: http://www.pnas.org/ cgi/doi/10.1073/pnas.0335320100. Cited 17 Oct 2017.

6. Russell JA, Moran NA. Costs and benefits of symbiont infection in aphids: variation among symbionts and across temperatures. Proc Biol Sci. 2006;273: 603-10 Available from: http://www.ncbi.nlm.nih.gov/pubmed/ 16537132%5Cn http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid= PMC1560055%5Cn http://rspb.royalsocietypublishing.org.gate1.inist.fr/ content/273/1586/603.short. Cited 17 Oct 2017.

7. Christian N, Whitaker BK, Clay K. Microbiomes: unifying animal and plant systems through the lens of community ecology theory. Front Microbiol. 2015;6:869 Frontiers. Available from: http://journal.frontiersin.org/Article/10. 3389/fmicb.2015.00869/abstract. Cited 18 Apr 2018.

8. McFall-Ngai M, Hadfield MG, Bosch TCG, Carey HV, Domazet-Lošo T, Douglas AE, et al. Animals in a bacterial world, a new imperative for the life sciences. Proc Natl Acad Sci. 2013;110:3229-36 National Academy of Sciences. Available from: http://www.pnas.org/lookup/doi/10.1073/pnas. 1218525110. Cited 18 Apr 2018.

9. Rosenberg E, Koren O, Reshef L, Efrony R, Zilber-Rosenberg I. The role of microorganisms in coral health, disease and evolution. Nat Rev Microbiol. 2007;5:355-62 Available from: http://www.nature.com/doifinder/10.1038/ nrmicro1635.

10. Rohwer F, Seguritan V, Azam F, Knowlton N. Diversity and distribution of coral-associated bacteria. Mar Ecol Prog Ser. 2002;243:1-10.

11. Bordenstein SR, Theis KR. Host biology in light of the microbiome: ten principles of holobionts and hologenomes. PLoS Biol. 2015;13:e1002226 Waldor MK, editor. Cambridge University Press. Available from: http://dx. plos.org/10.1371/journal.pbio.1002226. Cited 15 Oct 2017. [OpenAIRE]

12. Douglas AE, Werren JH. Holes in the hologenome: why host-microbe symbioses are not holobionts. MBio. 2016;7:e02099 American Society for Microbiology. Available from: http://www.ncbi.nlm.nih.gov/pubmed/ 27034285. Cited 5 Oct 2017.

13. Douglas AE. How multi-partner endosymbioses function. Nat Rev Microbiol. 2016;14:731-43 Available from: http://www.nature.com/doifinder/10.1038/ nrmicro.2016.151. Cited 15 Nov 2017.

14. Jaspers E, Overmann J. Ecological significance of microdiversity: identical 16S rRNA gene sequences can be found in bacteria with highly divergent genomes and ecophysiologies. Appl Environ Microbiol. 2004;70:4831-9 American Society for Microbiology. Available from: http://www.ncbi.nlm.nih. gov/pubmed/15294821. Cited 5 Oct 2017.

15. Thomas GH, Zucker J, Macdonald SJ, Sorokin A, Goryanin I, Douglas AE. A fragile metabolic network adapted for cooperation in the symbiotic bacterium Buchnera aphidicola. BMC Syst Biol. 2009;3:24 BioMed Central. Available from: http://bmcsystbiol.biomedcentral.com/articles/10.1186/1752- 0509-3-24. Cited 17 Nov 2017.

93 references, page 1 of 7
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