Molecular dissection of nutrient exchange at the insectmicrobial interface

Current Opinion in Insect Science

Volumn 4, Issue 1, 2014, Pages 23-28

  Douglas, Angela E ^a,b  

^a Cornell University ^*  (United States)

^b Department of Molecular Biology and Genetics ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HEXAPODA;

EID: 84925382591     PISSN: 22145745     EISSN: 22145753     Source Type: Journal    
DOI: 10.1016/j.cois.2014.08.007     Document Type: Review

References (45)

1. Buchner P: Endosymbioses of Animals with Plant Microorganisms. Chichester, UK: John Wiley and Sons; 1965,.
2. Douglas AE: Mycetocyte symbiosis in insects. Biol Rev Camb Philos Soc 1989, 64:409-434.
3. Roth LE, Jeon K, Stacey G: Homology in endosymbioti systems: the term 'symbiosome'. In Molecular Genetics of Plant-Microbe I2n2t0e-ra2c2t5io. ns. Edited by Palacios R, Verma DPS. APS Press; 1988
4. Udvardi M, Poole PS: Transport and metabolism in legumerhizobia symbioses. Annu Rev Plant Biol 2013, 64:781-805.
5. Shigenobu S, Wilson AC: Genomic revelations of a mutualism: the pea aphid and its obligate bacterial symbiont. Cell Mol Life Sci 2011, 68:1297-1309.
6. Macdonald SJ, Lin GG, Russell CW, Thomas GH, Douglas AE: The central role of the host cell in symbiotic nitrogen metabolism. Proc Biol Sci 2012, 279:2965-2973.
7. 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.
8. Tamas I, Klasson L, Canback B, Naslund AK, Eriksson AS, Wernegreen JJ, Sandstrom JP, Moran NA, Andersson SG: 50 million years of genomic stasis in endosymbiotic bacteria. Science 2002, 296:2376-2379.
9. Van Ham RC, Kamerbeek J, Palacios C, Rausell C, Abascal F, Bastolla U, Fernandez JM, Jimenez L, Postigo M, Silva FJ et al.: Reductive genome evolution in Buchnera aphidicola. Proc Natl Acad Sci U S A 2003, 100:581-586.
10. Hansen AK, Moran NA: Aphid genome expression reveals host-symbiont cooperation in the production of amino acids. Proc Natl Acad Sci U S A 2011, 108:2849-2854.
11. Poliakov A, Russell CW, Ponnala L, Hoops HJ, Sun Q, Douglas AE, Van Wijk KJ: Large-scale label-free quantitative proteomics of the pea aphid-Buchnera symbiosis. Mol Cell Proteomics 2011, 10 M110 007039.
12. Price DR, Duncan RP, Shigenobu S, Wilson AC: Genome expansion and differential expression of amino acid transporters at the aphid/Buchnera symbiotic interface. Mol Biol Evol 2011, 28:3113-3126.
13. Duncan RP, Husnik F, Van Leuven JT, Gilbert DG, Davalos LM, McCutcheon JP, Wilson AC: Dynamic recruitment of amino acid transporters to the insect/symbiont interface. Mol Ecol 2014, 23:1608-1623.
14. Shigenobu S, Watanabe H, Hattori M, Sakaki Y, Ishikawa H: Genome sequence of the endocellular bacterial symbiont of aphids Buchnera sp. APS. Nature 2000, 407:81-86.
15. Sabree ZL, Kambhampati S, Moran NA: Nitrogen recycling and nutritional provisioning by Blattabacterium, the cockroach endosymbiont. Proc Natl Acad Sci U S A 2009, 106:19521-19526.
16. McCutcheon JP, McDonald BR, Moran NA: Convergent evolution of metabolic roles in bacterial co-symbionts of insects. Proc Natl Acad Sci U S A 2009, 106:15394-15399.
17. McCutcheon JP, Von Dohlen CD: An interdependent metabolic patchwork in the nested symbiosis of mealybugs. Curr Biol 2011, 21:1366-1372.
18. McCutcheon JP, Moran NA: Functional convergence in reduced genomes of bacterial symbionts spanning 200 My ofevolution. Genome Biol Evol 2010, 2:708-718.
19. Sloan DB, Moran NA: Endosymbiotic bacteria as a source of carotenoids in whiteflies. Biol Lett 2012, 8:986-989.
20. Moran NA, Tran P, Gerardo NM: Symbiosis and insect diversification: an ancient symbiont of sap-feeding insects from the bacterial phylum Bacteroidetes. Appl Environ Microbiol 2005, 71:8802-8810.
21. Moran NA, Munson MA, Baumann P, Ishikawa H: A molecular clock in endosymbiotic bacteria is calibrated using the insect hosts. Proc Biol Sci 1993, 253:167-171.
22. Fares MA, Moya A, Barrio E: Adaptive evolution in GroEL from distantly related endosymbiotic bacteria of insects. J Evol Biol 2005, 18:651-660.
23. Stoll S, Feldhaar H, Gross R: Transcriptional profiling of the endosymbiont Blochmannia floridanus during different developmental stages of its holometabolous ant host. Environ Microbiol 2009, 11:877-888.
24. Ratzka C, Gross R, Feldhaar H: Gene expression analysis of the endosymbiont-bearing midgut tissue during ontogeny of the carpenter ant Camponotus floridanus. J Insect Physiol 2013, 59:611-623.
25. Russell CW, Bouvaine S, Newell PD, Douglas AE: Shared metabolic pathways in a coevolved insect-bacterial symbiosis. Appl Environ Microbiol 2013, 79:6117-6123. This study demonstrates that some reactions in essential amino acid synthesis are mediated by the aphid host, with the transport of metabolic intermediates across the host/bacterial interface.
26. Maezawa K, Shigenobu S, Taniguchi H, Kubo T, Aizawa S, Morioka M: Hundreds of flagellar basal bodies cover the cell surface of the endosymbiotic bacterium Buchnera aphidicola sp. strain APS. J Bacteriol 2006, 188:6539-6543.
27. Sasaki T, Ishikawa H: Production of essential amino acids from glutamate by mycetocyte symbionts of the pea aphid, Acyrthosiphon pisum. J Insect Physiol 1995, 41:41-46.
28. Price DR, Feng H, Baker JD, Bavan S, Luetje CW, Wilson AC: Aphid amino acid transporter regulates glutamine supply to intracellular bacterial symbionts. Proc Natl Acad Sci U S A 2014, 111:320-325. This study describes an aphid glutamine transporter that is subject to competitive inhibition by the essential amino acid arginine, providing the basis for regulation of nutrient exchange in the aphid-Buchnera symbiosis.
29. McCutcheon JP, Moran NA: Extreme genome reduction in symbiotic bacteria. Nat Rev Microbiol 2012, 10:13-26.
30. Moran NA: Accelerated evolution and Muller's rachet in endosymbiotic bacteria. Proc Natl Acad Sci U S A 1996, 93:2873-2878.
31. Nakabachi A, Yamashita A, Toh H, Ishikawa H, Dunbar HE, Moran NA, Hattori M: The 160-kilobase genome of the bacterial endosymbiont Carsonella. Science 2006, 314:267.
32. IAGC: Genome sequence of the pea aphid Acyrthosiphon pisum. PLoS Biol 2010, 8:e1000313.
33. Wilson AC, Ashton PD, Calevro F, Charles H, Colella S, Febvay G, Jander G, Kushlan PF, Macdonald SJ, Schwartz JF et al.: Genomic insight into the amino acid relations of the pea aphid, Acyrthosiphon pisum, with its symbiotic bacterium Buchnera aphidicola. Insect Mol Biol 2010, 19(Suppl. 2):249-258.
34. Husnik F, Nikoh N, Koga R, Ross L, Duncan RP, Fujie M, Tanaka M, Satoh N, Bachtrog D, Wilson AC Etal: Horizontal gene transfer from diverse bacteria to an insect genome enables a tripartite nested mealybug symbiosis. Cell 2013, 153:1567-1578. This study demonstrates that multiple bacterial genes are integrated into the mealybug genome, including genes contributing to essential amino acid biosynthesis.
35. Sloan DB, Nakabachi A, Richards S, Qu J, Murali SC, Gibbs RA, Moran NA: Parallel histories of horizontal gene transfer facilitated extreme reduction of endosymbiont genomes in sap-feeding insects. Mol Biol Evol 2014, 31:857-871. This study shows the likely transfer of a gene from the bacteriocyte symbiont Carsonella to the genome of its psyllid host.
36. Urban JM, Cryan JR: Two ancient bacterial endosymbionts have coevolved with the planthoppers (Insecta: Hemiptera: Fulgoroidea). BMC Evol Biol 2012, 12:87.
37. Bennett GM, Moran NA: Small, smaller, smallest: the origins and evolution of ancient dual symbioses in a Phloem-feeding insect. Genome Biol Evol 2013, 5:1675-1688.
38. i5k Consortium: The i5K initiative: advancing arthropod genomics for knowledge, human health, agriculture, and the environment. J Hered 2013, 104:595-600.
39. Lopez-Sanchez MJ, Neef A, Pereto J, Patino-Navarrete R, Pignatelli M, Latorre A, Moya A: Evolutionary convergence and nitrogen metabolism in Blattabacterium strain Bge, primary endosymbiont of the cockroach Blattella germanica. PLoS Genet 2009, 5:e1000721.
40. Wernegreen JJ, Kauppinen SN, Brady SG, Ward PS: One nutritional symbiosis begat another: phylogenetic evidence that the ant tribe Camponotini acquired Blochmannia by tending sap-feeding insects. BMC Evol Biol 2009, 9:292.
41. Toju H, Tanabe AS, Notsu Y, Sota T, Fukatsu T: Diversification of endosymbiosis: replacements, co-speciation and promiscuity of bacteriocyte symbionts in weevils. ISME J 2013, 7:1378-1390. This study reports repeated evolutionary shifts in bacteriocyte symbionts of weevils, demonstrating that metabolic coevolution may not result in absolute host dependence on specific microbial symbiont (s).
42. Koga R, Bennett GM, Cryan JR, Moran NA: Evolutionary replacement of obligate symbionts in an ancient and diverse insect lineage. Environ Microbiol 2013, 15:2073-2081.
43. Toenshoff ER, Gruber D, Horn M: Co-evolution and symbiont replacement shaped the symbiosis between adelgids (Hemiptera: Adelgidae) and their bacterial symbionts. Environ Microbiol 2012, 14:1284-1295.
44. Perez-Brocal V, Gil R, Ramos S, Lamelas A, Postigo M, Michelena JM, Silva FJ, Moya A, Latorre A: A small microbial genome: the end of a long symbiotic relationship? Science 2006, 314:312-313.
45. Koga R, Tsuchida T, Fukatsu T: Changing partners in an obligate symbiosis: a facultative endosymbiont can compensate for loss of the essential endosymbiont Buchnera in an aphid. Proc Biol Sci 2003, 270:2543-2550.