Dynamic gut microbiome across life history of the malaria mosquito anopheles gambiae in Kenya

PLoS ONE

Volumn 6, Issue 9, 2011, Pages

  Wang, Ying ^a,c   Gilbreath III, Thomas M ^b   Kukutla, Phanidhar ^a   Yan, Guiyun ^b   Xu, Jiannong ^a  

^a NEW MEXICO STATE UNIVERSITY   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c THIRD MILITARY MEDICAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

RNA 16S; BACTERIAL RNA;

ANOPHELES GAMBIAE; ARTICLE; BACTEROIDETES; CATABOLISM; CONTROLLED STUDY; CYANOBACTERIUM; GENETIC ANALYSIS; HOMEOSTASIS; IMAGO; INSECT; INTESTINE FLORA; KENYA; LARVA; LIFE HISTORY; MICROBIAL COMMUNITY; MICROBIAL DIVERSITY; MICROBIOME; NITROSATIVE STRESS; NONHUMAN; OXIDATION REDUCTION REACTION; OXIDATIVE STRESS; PROTEOBACTERIA; PYROSEQUENCING; SEQUENCE ANALYSIS; ANIMAL; ANIMAL FOOD; BACTERIUM; DISEASE CARRIER; DISEASE TRANSMISSION; FEMALE; GASTROINTESTINAL TRACT; GENETICS; GROWTH, DEVELOPMENT AND AGING; HUMAN; ISOLATION AND PURIFICATION; LABORATORY; LIFE CYCLE STAGE; MALARIA; METAGENOME; METAGENOMICS; MICROBIOLOGY;

ANOPHELES GAMBIAE; BACTERIA (MICROORGANISMS); BACTEROIDETES; CYANOBACTERIA; ENTEROBACTERIACEAE; FLAVOBACTERIACEAE; PROTEOBACTERIA;

ANIMAL FEED; ANIMALS; ANOPHELES GAMBIAE; BACTERIA; FEMALE; GASTROINTESTINAL TRACT; HUMANS; INSECT VECTORS; KENYA; LABORATORIES; LIFE CYCLE STAGES; MALARIA; METAGENOME; METAGENOMICS; OXIDATION-REDUCTION; RNA, BACTERIAL; RNA, RIBOSOMAL, 16S; SEQUENCE ANALYSIS, RNA;

EID: 80053001966     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0024767     Document Type: Article

References (83)

1. Warnecke F, Luginbuhl P, Ivanova N, Ghassemian M, Richardson TH, et al. (2007) Metagenomic and functional analysis of hindgut microbiota of a wood-feeding higher termite. Nature 450: 560-565.
2. Tartar A, Wheeler MM, Zhou X, Coy MR, Boucias DG, et al. (2009) Parallel metatranscriptome analyses of host and symbiont gene expression in the gut of the termite Reticulitermes flavipes. Biotechnol Biofuels 2: 25.
3. Suen G, Scott JJ, Aylward FO, Adams SM, Tringe SG, et al. (2010) An insect herbivore microbiome with high plant biomass-degrading capacity. PLoS Genet 6.
4. Dillon RJ, Dillon VM, (2004) The gut bacteria of insects: nonpathogenic interactions. Annu Rev Entomol 49: 71-92.
5. Gonzalez-Ceron L, Santillan F, Rodriguez MH, Mendez D, Hernandez-Avila JE, (2003) Bacteria in midguts of field-collected Anopheles albimanus block Plasmodium vivax sporogonic development. J Med Entomol 40: 371-374.
6. Pumpuni CB, Demaio J, Kent M, Davis JR, Beier JC, (1996) Bacterial population dynamics in three anopheline species: the impact on Plasmodium sporogonic development. Am J Trop Med Hyg 54: 214-218.
7. Straif SC, Mbogo CN, Toure AM, Walker ED, Kaufman M, et al. (1998) Midgut bacteria in Anopheles gambiae and An. funestus (Diptera: Culicidae) from Kenya and Mali. J Med Entomol 35: 222-226.
8. Terenius O, de Oliveira CD, Pinheiro WD, Tadei WP, James AA, et al. (2008) 16S rRNA gene sequences from bacteria associated with adult Anopheles darlingi (Diptera: Culicidae) mosquitoes. J Med Entomol 45: 172-175.
9. Lindh JM, Terenius O, Faye I, (2005) 16S rRNA gene-based identification of midgut bacteria from field-caught Anopheles gambiae sensu lato and A. funestus mosquitoes reveals new species related to known insect symbionts. Appl Environ Microbiol 71: 7217-7223.
10. Rani A, Sharma A, Rajagopal R, Adak T, Bhatnagar RK, (2009) Bacterial diversity analysis of larvae and adult midgut microflora using culture-dependent and culture-independent methods in lab-reared and field-collected Anopheles stephensi-an Asian malarial vector. Bmc Microbiology 9.
11. Gusmao DS, Santos AV, Marini DC, Bacci M Jr, Berbert-Molina MA, et al. (2010) Culture-dependent and culture-independent characterization of microorganisms associated with Aedes aegypti (Diptera: Culicidae) (L.) and dynamics of bacterial colonization in the midgut. Acta Trop 115: 275-281.
12. Pidiyar VJ, Jangid K, Patole MS, Shouche YS, (2004) Studies on cultured and uncultured microbiota of wild culex quinquefasciatus mosquito midgut based on 16s ribosomal RNA gene analysis. Am J Trop Med Hyg 70: 597-603.
13. Damiani C, Ricci I, Crotti E, Rossi P, Rizzi A, et al. (2010) Mosquito-bacteria symbiosis: the case of Anopheles gambiae and Asaia. Microb Ecol 60: 644-654.
14. Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, et al. (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75: 7537-7541.
15. Wang Q, Garrity GM, Tiedje JM, Cole JR, (2007) Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73: 5261-5267.
16. Vazquez-Martinez MG, Rodriguez MH, Arredondo-Jimenez JI, Mendez-Sanchez JD, Bond-Compean JG, et al. (2002) Cyanobacteria associated with Anopheles albimanus (Diptera: Culicidae) larval habitats in southern Mexico. J Med Entomol 39: 825-832.
17. Thiery I, Nicolas L, Rippka R, Tandeau de Marsac N, (1991) Selection of cyanobacteria isolated from mosquito breeding sites as a potential food source for mosquito larvae. Appl Environ Microbiol 57: 1354-1359.
18. Kampfer P, Lindh JM, Terenius O, Haghdoost S, Falsen E, et al. (2006) Thorsellia anophelis gen. nov., sp. nov., a new member of the Gammaproteobacteria. Int J Syst Evol Microbiol 56: 335-338.
19. Briones AM, Shililu J, Githure J, Novak R, Raskin L, (2008) Thorsellia anophelis is the dominant bacterium in a Kenyan population of adult Anopheles gambiae mosquitoes. ISME J 2: 74-82.
20. Moll RM, Romoser WS, Modrzakowski MC, Moncayo AC, Lerdthusnee K, (2001) Meconial peritrophic membranes and the fate of midgut bacteria during mosquito (Diptera: Culicidae) metamorphosis. J Med Entomol 38: 29-32.
21. Romoser WS, Moll RM, Moncayo AC, Lerdthusnee K, (2000) The occurrence and fate of the meconium and meconial peritrophic membranes in pupal and adult mosquitoes (Diptera: Culicidae). J Med Entomol 37: 893-896.
22. Lindh JM, Borg-Karlson AK, Faye I, (2008) Transstadial and horizontal transfer of bacteria within a colony of Anopheles gambiae (Diptera: Culicidae) and oviposition response to bacteria-containing water. Acta Trop 107: 242-250.
23. Linser PJ, Smith KE, Seron TJ, Neira Oviedo M, (2009) Carbonic anhydrases and anion transport in mosquito midgut pH regulation. J Exp Biol 212: 1662-1671.
24. Kajla MK, Andreeva O, Gilbreath TM 3rd, Paskewitz SM, (2010) Characterization of expression, activity and role in antibacterial immunity of Anopheles gambiae lysozyme c-1. Comp Biochem Physiol B Biochem Mol Biol 155: 201-209.
25. Foster WA, (1995) Mosquito sugar feeding and reproductive energetics. Annu Rev Entomol 40: 443-474.
26. Briegel H, (1990) Fecundity, metabolism, and body size in Anopheles (Diptera: Culicidae), vectors of malaria. J Med Entomol 27: 839-850.
27. Foster WA, Takken W, (2004) Nectar-related vs. human-related volatiles: behavioural response and choice by female and male Anopheles gambiae (Diptera: Culicidae) between emergence and first feeding. Bull Entomol Res 94: 145-157.
28. Gary RE Jr, Foster WA, (2004) Anopheles gambiae feeding and survival on honeydew and extra-floral nectar of peridomestic plants. Med Vet Entomol 18: 102-107.
29. Impoinvil DE, Kongere JO, Foster WA, Njiru BN, Killeen GF, et al. (2004) Feeding and survival of the malaria vector Anopheles gambiae on plants growing in Kenya. Med Vet Entomol 18: 108-115.
30. Manda H, Gouagna LC, Nyandat E, Kabiru EW, Jackson RR, et al. (2007) Discriminative feeding behaviour of Anopheles gambiae s.s. on endemic plants in western Kenya. Med Vet Entomol 21: 103-111.
31. Gonzalez-Teuber M, Heil M, (2009) Nectar chemistry is tailored for both attraction of mutualists and protection from exploiters. Plant Signal Behav 4: 809-813.
32. Sacktor B, Wormser-Shavit E, (1966) Regulation of Metabolism in Working Muscle in Vivo. Journal of Biological Chemistry 241: 624-631.
33. Scaraffia PY, Wells MA, (2003) Proline can be utilized as an energy substrate during flight of Aedes aegypti females. J Insect Physiol 49: 591-601.
34. Morris RM, Rappe MS, Connon SA, Vergin KL, Siebold WA, et al. (2002) SAR11 clade dominates ocean surface bacterioplankton communities. Nature 420: 806-810.
35. Giovannoni SJ, Tripp HJ, Givan S, Podar M, Vergin KL, et al. (2005) Genome streamlining in a cosmopolitan oceanic bacterium. Science 309: 1242-1245.
36. Koch AL, (2001) Oligotrophs versus copiotrophs. Bioessays 23: 657-661.
37. Kumar S, Christophides GK, Cantera R, Charles B, Han YS, et al. (2003) The role of reactive oxygen species on Plasmodium melanotic encapsulation in Anopheles gambiae. Proc Natl Acad Sci U S A 100: 14139-14144.
38. Souza AV, Petretski JH, Demasi M, Bechara EJ, Oliveira PL, (1997) Urate protects a blood-sucking insect against hemin-induced oxidative stress. Free Radic Biol Med 22: 209-214.
39. Toh SQ, Glanfield A, Gobert GN, Jones MK, (2010) Heme and blood-feeding parasites: friends or foes? Parasit Vectors 3: 108.
40. Luckhart S, Vodovotz Y, Cui L, Rosenberg R, (1998) The mosquito Anopheles stephensi limits malaria parasite development with inducible synthesis of nitric oxide. Proc Natl Acad Sci U S A 95: 5700-5705.
41. Peterson TM, Gow AJ, Luckhart S, (2007) Nitric oxide metabolites induced in Anopheles stephensi control malaria parasite infection. Free Radic Biol Med 42: 132-142.
42. Peterson TM, Luckhart S, (2006) A mosquito 2-Cys peroxiredoxin protects against nitrosative and oxidative stresses associated with malaria parasite infection. Free Radic Biol Med 40: 1067-1082.
43. Graca-Souza AV, Maya-Monteiro C, Paiva-Silva GO, Braz GR, Paes MC, et al. (2006) Adaptations against heme toxicity in blood-feeding arthropods. Insect Biochem Mol Biol 36: 322-335.
44. Lehane MJ, (1997) Peritrophic matrix structure and function. Annu Rev Entomol 42: 525-550.
45. Devenport M, Alvarenga PH, Shao L, Fujioka H, Bianconi ML, et al. (2006) Identification of the Aedes aegypti peritrophic matrix protein AeIMUCI as a heme-binding protein. Biochemistry 45: 9540-9549.
46. Pascoa V, Oliveira PL, Dansa-Petretski M, Silva JR, Alvarenga PH, et al. (2002) Aedes aegypti peritrophic matrix and its interaction with heme during blood digestion. Insect Biochem Mol Biol 32: 517-523.
47. Demaio J, Pumpuni CB, Kent M, Beier JC, (1996) The midgut bacterial flora of wild Aedes triseriatus, Culex pipiens, and Psorophora columbiae mosquitoes. Am J Trop Med Hyg 54: 219-223.
48. Lushchak VI, (2011) Adaptive response to oxidative stress: Bacteria, fungi, plants and animals. Comp Biochem Physiol C Toxicol Pharmacol 153: 175-190.
49. Pomposiello PJ, Bennik MH, Demple B, (2001) Genome-wide transcriptional profiling of the Escherichia coli responses to superoxide stress and sodium salicylate. J Bacteriol 183: 3890-3902.
50. Dietrich LE, Teal TK, Price-Whelan A, Newman DK, (2008) Redox-active antibiotics control gene expression and community behavior in divergent bacteria. Science 321: 1203-1206.
51. Zheng M, Aslund F, Storz G, (1998) Activation of the OxyR transcription factor by reversible disulfide bond formation. Science 279: 1718-1721.
52. Hishinuma S, Ohtsu I, Fujimura M, Fukumori F, (2008) OxyR is involved in the expression of thioredoxin reductase TrxB in Pseudomonas putida. FEMS Microbiol Lett 289: 138-145.
53. Hishinuma S, Yuki M, Fujimura M, Fukumori F, (2006) OxyR regulated the expression of two major catalases, KatA and KatB, along with peroxiredoxin, AhpC in Pseudomonas putida. Environ Microbiol 8: 2115-2124.
54. Kim SO, Merchant K, Nudelman R, Beyer WF Jr, Keng T, et al. (2002) OxyR: a molecular code for redox-related signaling. Cell 109: 383-396.
55. Spiro S, (2006) Nitric oxide-sensing mechanisms in Escherichia coli. Biochem Soc Trans 34: 200-202.
56. D'Autreaux B, Tucker NP, Dixon R, Spiro S, (2005) A non-haem iron centre in the transcription factor NorR senses nitric oxide. Nature 437: 769-772.
57. Bush M, Ghosh T, Tucker N, Zhang X, Dixon R, (2011) Transcriptional regulation by the dedicated nitric oxide sensor, NorR: a route towards NO detoxification. Biochem Soc Trans 39: 289-293.
58. Mukhopadhyay P, Zheng M, Bedzyk LA, LaRossa RA, Storz G, (2004) Prominent roles of the NorR and Fur regulators in the Escherichia coli transcriptional response to reactive nitrogen species. Proc Natl Acad Sci U S A 101: 745-750.
59. Schopfer MP, Wang J, Karlin KD, (2010) Bioinspired heme, heme/nonheme diiron, heme/copper, and inorganic NOx chemistry: *NO((g)) oxidation, peroxynitrite-metal chemistry, and *NO((g)) reductive coupling. Inorg Chem 49: 6267-6282.
60. Gardner PR, (2005) Nitric oxide dioxygenase function and mechanism of flavohemoglobin, hemoglobin, myoglobin and their associated reductases. J Inorg Biochem 99: 247-266.
61. Bonamore A, Boffi A, (2008) Flavohemoglobin: structure and reactivity. IUBMB Life 60: 19-28.
62. Cruz-Ramos H, Crack J, Wu G, Hughes MN, Scott C, et al. (2002) NO sensing by FNR: regulation of the Escherichia coli NO-detoxifying flavohaemoglobin, Hmp. EMBO J 21: 3235-3244.
63. Bodenmiller DM, Spiro S, (2006) The yjeB (nsrR) gene of Escherichia coli encodes a nitric oxide-sensitive transcriptional regulator. J Bacteriol 188: 874-881.
64. Gardner PR, Gardner AM, Martin LA, Salzman AL, (1998) Nitric oxide dioxygenase: an enzymic function for flavohemoglobin. Proc Natl Acad Sci U S A 95: 10378-10383.
65. Gardner PR, Costantino G, Salzman AL, (1998) Constitutive and adaptive detoxification of nitric oxide in Escherichia coli. Role of nitric-oxide dioxygenase in the protection of aconitase. J Biol Chem 273: 26528-26533.
66. Poole RK, (2005) Nitric oxide and nitrosative stress tolerance in bacteria. Biochem Soc Trans 33: 176-180.
67. Kumar S, Molina-Cruz A, Gupta L, Rodrigues J, Barillas-Mury C, (2010) A peroxidase/dual oxidase system modulates midgut epithelial immunity in Anopheles gambiae. Science 327: 1644-1648.
68. Oliveira JH, Goncalves RL, Lara FA, Dias FA, Gandara AC, et al. (2011) Blood Meal-Derived Heme Decreases ROS Levels in the Midgut of Aedes aegypti and Allows Proliferation of Intestinal Microbiota. PLoS Pathog 7: e1001320.
69. Dong Y, Manfredini F, Dimopoulos G, (2009) Implication of the mosquito midgut microbiota in the defense against malaria parasites. PLoS Pathog 5: e1000423.
70. Riehle MA, Moreira CK, Lampe D, Lauzon C, Jacobs-Lorena M, (2007) Using bacteria to express and display anti-Plasmodium molecules in the mosquito midgut. Int J Parasitol 37: 595-603.
71. Coutinho-Abreu IV, Zhu KY, Ramalho-Ortigao M, (2010) Transgenesis and paratransgenesis to control insect-borne diseases: current status and future challenges. Parasitol Int 59: 1-8.
72. Sogin ML, Morrison HG, Huber JA, Mark Welch D, Huse SM, et al. (2006) Microbial diversity in the deep sea and the underexplored "rare biosphere". Proc Natl Acad Sci U S A 103: 12115-12120.
73. Dowd SE, Callaway TR, Wolcott RD, Sun Y, McKeehan T, et al. (2008) Evaluation of the bacterial diversity in the feces of cattle using 16S rDNA bacterial tag-encoded FLX amplicon pyrosequencing (bTEFAP). BMC Microbiol 8: 125.
74. Andreotti R, Perez de Leon AA, Dowd SE, Guerrero FD, Bendele KG, et al. (2011) Assessment of bacterial diversity in the cattle tick Rhipicephalus (Boophilus) microplus through tag-encoded pyrosequencing. BMC Microbiol 11: 6.
75. Schloss PD, (2010) The effects of alignment quality, distance calculation method, sequence filtering, and region on the analysis of 16S rRNA gene-based studies. PLoS Comput Biol 6: e1000844.
76. Pruesse E, Quast C, Knittel K, Fuchs BM, Ludwig W, et al. (2007) SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Res 35: 7188-7196.
77. Chao A, Yang MCK, (1993) Stopping rules and estimation for recapture debugging with unequal failure rates. Biometrika 80: 193-201.
78. Chao A, Lee S-M, (1992) Estimating the number of classes via sample coverage. J Am Stat Assoc 87: 210-217.
79. Chao A, (1984) Nonparametric estimation of the number of classes in a population. Scand J Statist 11: 165-270.
80. Gotelli NJ, Colwell RK, (2001) Quantifying biodiversity: procedures and pitfalls in the measurement and comparison of species richness. Ecol Lett 4: 379-391.
81. White JR, Nagarajan N, Pop M, (2009) Statistical Methods for Detecting Differentially Abundant Features in Clinical Metagenomic Samples. PLoS Comput Biol 5: e1000352.
82. Aziz RK, Bartels D, Best AA, DeJongh M, Disz T, et al. (2008) The RAST Server: rapid annotations using subsystems technology. BMC Genomics 9: 75.
83. Lehman RM, Lundgren JG, Petzke LM, (2009) Bacterial communities associated with the digestive tract of the predatory ground beetle, Poecilus chalcites, and their modification by laboratory rearing and antibiotic treatment. Microb Ecol 57: 349-358.