Planta Med 2021; 87(01/02): 38-48
DOI: 10.1055/a-1229-9435
Biological and Pharmacological Activities
Reviews

Chemical Ecology in Insect-microbe Interactions in the Neotropics

Departamento de Ciências Farmacêuticas, Faculdade de Ciências Farmacêuticas de Ribeirão Preto, Universidade de São Paulo, Ribeirão Preto, Brazil
,
Departamento de Ciências Farmacêuticas, Faculdade de Ciências Farmacêuticas de Ribeirão Preto, Universidade de São Paulo, Ribeirão Preto, Brazil
,
Departamento de Ciências Farmacêuticas, Faculdade de Ciências Farmacêuticas de Ribeirão Preto, Universidade de São Paulo, Ribeirão Preto, Brazil
› Author Affiliations
Supported by: Coordenação de Aperfeiçoamento de Pessoal de Nível Superior Finance Code 001
Supported by: Fundação de Amparo à Pesquisa do Estado de São Paulo 2013/07600-3
Supported by: Fundação de Amparo à Pesquisa do Estado de São Paulo 2013/50954-0
Supported by: Fundação de Amparo à Pesquisa do Estado de São Paulo 2015/26349-5
Supported by: Fundação de Amparo à Pesquisa do Estado de São Paulo 2016/15576-3
Supported by: Conselho Nacional de Desenvolvimento Científico e Tecnológico 303792/2018-2

Abstract

Small molecules frequently mediate symbiotic interactions between microorganisms and their hosts. Brazil harbors the highest diversity of insects in the world; however, just recently, efforts have been directed to deciphering the chemical signals involved in the symbioses of microorganisms and social insects. The current scenario of natural products research guided by chemical ecology is discussed in this review. Two groups of social insects have been prioritized in the studies, fungus-farming ants and stingless bees, leading to the identification of natural products involved in defensive and nutritional symbioses. Some of the compounds also present potential pharmaceutical applications as antimicrobials, and this is likely related to their ecological roles. Microbial symbioses in termites and wasps are suggested promising sources of biologically active small molecules. Aspects related to public policies for insect biodiversity preservation are also highlighted.



Publication History

Received: 29 May 2020

Accepted after revision: 29 July 2020

Article published online:
27 August 2020

© 2020. Thieme. All rights reserved.

Georg Thieme Verlag KG
Rüdigerstraße 14, 70469 Stuttgart, Germany

 
  • References

  • 1 Mittermeier RA, Da Fonseca GAB, Rylands AB, Brandon K. A brief history of biodiversity conservation in Brazil. Conserv Biol 2005; 19: 601-607
  • 2 Pinto AC, Silva DHS, Bolzani VD, Lopes NP, Epifanio RD. Current status, challenges and trends on natural products in Brazil. Quim Nova 2002; 25: 45-61
  • 3 Berlinck RGS, Borges WD, Scotti MT, Vieira PC. The chemistry of natural products in Brazil in the XXI century. Quim Nova 2017; 40: 706-710
  • 4 de Oliveira LG, Pupo MT, Vieira PC. Exploring microbial natural products in the frontiers of chemistry and biology. Quim Nova 2013; 36: 1577-1586
  • 5 Ioca LP, Allard PM, Berlinck RGS. Thinking big about small beings–the (yet) underdeveloped microbial natural products chemistry in Brazil. Nat Prod Rep 2014; 31: 646-675
  • 6 Castelle CJ, Banfield JF. Major new microbial groups expand diversity and alter our understanding of the tree of life. Cell 2018; 172: 1181-1197
  • 7 Charlop-Powers Z, Owen JG, Reddy BVB, Ternei M, Guimaraes DO, de Frias UA, Pupo MT, Seepe P, Feng ZY, Brady SF. Global biogeographic sampling of bacterial secondary metabolism. Elife 2015; 4: e05048
  • 8 Moran NA. Symbiosis. Curr Biol 2006; 16: R866-R871
  • 9 Wilkinson DM. At cross purposes–how do we cope with scientific terms that have two different definitions?. Nature 2001; 412: 485
  • 10 Russell JA, Sanders JG, Moreau CS. Hotspots for symbiosis: function, evolution, and specificity of ant-microbe associations from trunk to tips of the ant phylogeny (Hymenoptera: Formicidae). Myrmecol News 2017; 24: 43-69
  • 11 Mithofer A, Boland W. Do you speak chemistry? Small chemical compounds represent the evolutionary oldest form of communication between organisms. EMBO Rep 2016; 17: 626-629
  • 12 Bergstrom G. Chemical ecology = chemistry plus ecology!. Pure Appl Chem 2007; 79: 2305-2323
  • 13 Stork NE. How many species of insects and other terrestrial arthropods are there on earth?. Annu Rev Entomol 2018; 63: 31-45
  • 14 Rafael JA, Aguiar AP, Amorim DD. Knowledge of insect diversity in Brazil: challenges and advances. Neotrop Entomol 2009; 38: 565-570
  • 15 Bergmann J, Gonzalez A, Zarbin PHG. Insect pheromone research in South America. J Brazil Chem Soc 2009; 20: 1206-1219
  • 16 Wilson EO, Holldobler B. Eusociality: origin and consequences. P Natl Acad Sci USA 2005; 102: 13367-13371
  • 17 Ramadhar TR, Beemelmanns C, Currie CR, Clardy J. Bacterial symbionts in agricultural systems provide a strategic source for antibiotic discovery. J Antibiot 2014; 67: 53-58
  • 18 Biedermann PHW, Vega FE. Ecology and evolution of insect-fungus mutualisms. Annu Rev Entomol 2020; 65: 431-455
  • 19 Evans JD, Aronstein K, Chen YP, Hetru C, Imler JL, Jiang H, Kanost M, Thompson GJ, Zou Z, Hultmark D. Immune pathways and defence mechanisms in honey bees Apis mellifera . Insect Mol Biol 2006; 15: 645-656
  • 20 Van Arnam EB, Currie CR, Clardy J. Defense contracts: molecular protection in insect-microbe symbioses. Chem Soc Rev 2018; 47: 1638-1651
  • 21 Fukuda TTH, Cassilly CD, Gerdt JP, Henke MT, Helfrich EJN, Mevers E. Research tales from the Clardy laboratory: function-driven natural product discovery. J Nat Prod 2020; 83: 744-755
  • 22 Chevrette MG, Carlson CM, Ortega HE, Thomas C, Ananiev GE, Barns KJ, Book AJ, Cagnazzo J, Carlos C, Flanigan W, Grubbs KJ, Horn HA, Hoffmann FM, Klassen JL, Knack JJ, Lewin GR, McDonald BR, Muller L, Melo WGP, Pinto-Tomas AA, Schmitz A, Wendt-Pienkowski E, Wildman S, Zhao M, Zhang F, Bugni TS, Andes DR, Pupo MT, Currie CR. The antimicrobial potential of Streptomyces from insect microbiomes. Nat Commun 2019; 10: 516
  • 23 Wilson EO. Sociobiology: The new Synthesis. Cambridge: Harvard University Press; 1975
  • 24 Hölldobler B, Wilson EO. The Ants. Cambridge: Harvard University Press; 1990: 596
  • 25 Branstetter MG, Jesovnik A, Sosa-Calvo J, Lloyd MW, Faircloth BC, Brady SG, Schultz TR. Dry habitats were crucibles of domestication in the evolution of agriculture in ants. P Roy Soc B-Biol Sci 2017; 284: 20170095
  • 26 Schultz TR, Brady SG. Major evolutionary transitions in ant agriculture. P Natl Acad Sci USA 2008; 105: 5435-5440
  • 27 Currie CR, Mueller UG, Malloch D. The agricultural pathology of ant fungus gardens. P Natl Acad Sci USA 1999; 96: 7998-8002
  • 28 Currie CR, Scott JA, Summerbell RC, Malloch D. Fungus-growing ants use antibiotic-producing bacteria to control garden parasites. Nature 1999; 398: 701-704
  • 29 Cafaro MJ, Currie CR. Phylogenetic analysis of mutualistic filamentous bacteria associated with fungus-growing ants. Can J Microbiol 2005; 51: 441-446
  • 30 Oh DC, Poulsen M, Currie CR, Clardy J. Dentigerumycin: a bacterial mediator of an ant-fungus symbiosis. Nat Chem Biol 2009; 5: 391-393
  • 31 Carr G, Derbyshire ER, Caldera E, Currie CR, Clardy J. Antibiotic and antimalarial quinones from fungus-growing ant-associated Pseudonocardia sp. J Nat Prod 2012; 75: 1806-1809
  • 32 Sit CS, Ruzzini AC, Van Arnam EB, Ramadhar TR, Currie CR, Clardy J. Variable genetic architectures produce virtually identical molecules in bacterial symbionts of fungus-growing ants. P Natl Acad Sci USA 2015; 112: 13150-13154
  • 33 Van Arnam EB, Ruzzini AC, Sit CS, Currie CR, Clardy J. A Rebeccamycin analog provides plasmid-encoded niche defense. J Am Chem Soc 2015; 137: 14272-14274
  • 34 Van Arnam EB, Ruzzini AC, Sit CS, Horn H, Pinto-Tomas AA, Currie CR, Clardy J. Selvamicin, an atypical antifungal polyene from two alternative genomic contexts. P Natl Acad Sci USA 2016; 113: 12940-12945
  • 35 Marsh SE, Poulsen M, Gorosito NB, Pinto-Tomas A, Masiulionis VE, Currie CR. Association between Pseudonocardia symbionts and Atta leaf-cutting ants suggested by improved isolation methods. Int Microbiol 2013; 16: 17-25
  • 36 Carreiro SC, Pagnocca FC, Bacci M, Bueno OC, Hebling MJA, Middelhoven WJ. Occurrence of killer yeasts in leaf-cutting ant nests. Folia Microbiol 2002; 47: 259-262
  • 37 Santos AV, Dillon RJ, Dillon VM, Reynolds SE, Samuels RI. Ocurrence of the antibiotic producing bacterium Burkholderia sp in colonies of the leaf-cutting ant Atta sexdens rubropilosa. FEMS Microbiol Lett 2004; 239: 319-323
  • 38 Silva-Junior EA, Ruzzini AC, Paludo CR, Nascimento FS, Currie CR, Clardy J, Pupo MT. Pyrazines from bacteria and ants: convergent chemistry within an ecological niche. Sci Rep 2018; 8: 1-7
  • 39 Engl T, Kaltenpoth M. Influence of microbial symbionts on insect pheromones. Nat Prod Rep 2018; 35: 386-397
  • 40 Silva-Junior EA, Paludo CR, Valadares L, Lopes NP, do Nascimento FS, Pupo MT. Aflatoxins produced by Aspergillus nomius ASR3, a pathogen isolated from the leaf-cutter ant Atta sexdens rubropilosa . Rev Bras Farmacogn 2017; 27: 529-532
  • 41 Zucchi TD, Guidolin AS, Consoli FL. Isolation and characterization of actinobacteria ectosymbionts from Acromyrmex subterraneus brunneus (Hymenoptera, Formicidae). Microbiol Res 2011; 166: 68-76
  • 42 Van der Meij A, Worsley SF, Hutchings MI, van Wezel GP. Chemical ecology of antibiotic production by actinomycetes. FEMS Microbiol Rev 2017; 41: 392-416
  • 43 Mendes TD, Borges WS, Rodrigues A, Solomon SE, Vieira PC, Duarte MCT, Pagnocca FC. Anti-Candida properties of urauchimycins from actinobacteria associated with Trachymyrmex ants. Biomed Res Int 2013; 2013: 1-8
  • 44 Pupo MT, Currie CR, Clardy J. Microbial symbionts of insects are the focus of the first international cooperative biodiversity group (ICBG) in Brazil. J Brazil Chem Soc 2017; 28: 393-401
  • 45 Ortega HE, Batista JM, Melo WGP, de Paula GT, Pupo MT. Structure and absolute configuration of secondary metabolites from two strains of Streptomyces chartreusis associated with attine ants. J Brazil Chem Soc 2019; 30: 2672-2680
  • 46 Ortega HE, Batista JM, Melo WGP, Clardy J, Pupo MT. Absolute configurations of griseorhodins A and C. Tetrahedron Lett 2017; 58: 4721-4723
  • 47 Ortega HE, Ferreira LLG, Melo WGP, Oliveira ALL, Alvarenga RFR, Lopes NP, Bugni TS, Andricopulo AD, Pupo MT. Antifungal compounds from Streptomyces associated with attine ants also inhibit Leishmania donovani . Plos Neglect Trop D 2019; 13: e0007643
  • 48 Morais PB, Calaça PSST, Rosa CA. Microorganisms associated with stingless Bees. In: Pot-Honey. Springer; 2013: 173-186
  • 49 Kwong WK, Moran NA. Gut microbial communities of social bees. Nat Rev Microbiol 2016; 14: 374
  • 50 Moran NA. Genomics of the honey bee microbiome. Curr Opin Insect Sci 2015; 10: 22-28
  • 51 Mattila HR, Rios D, Walker-Sperling VE, Roeselers G, Newton ILG. Characterization of the active microbiotas associated with honey bees reveals healthier and broader communities when colonies are genetically diverse. PLoS One 2012; 7: e32962
  • 52 Martinson VG, Danforth BN, Minckley RL, Rueppell O, Tingek S, Moran NA. A simple and distinctive microbiota associated with honey bees and bumble bees. Mol Ecol 2011; 20: 619-628
  • 53 Crotti E, Rizzi A, Chouaia B, Ricci I, Favia G, Alma A, Sacchi L, Bourtzis K, Mandrioli M, Cherif A, Bandi C, Daffonchio D. Acetic acid bacteria, newly emerging symbionts of insects. Appl Environ Microb 2010; 76: 6963-6970
  • 54 Florez LV, Biedermann PHW, Engl T, Kaltenpoth M. Defensive symbioses of animals with prokaryotic and eukaryotic microorganisms. Nat Prod Rep 2015; 32: 904-936
  • 55 Forsgren E, Olofsson TC, Vasquez A, Fries I. Novel lactic acid bacteria inhibiting Paenibacillus larvae in honey bee larvae. Apidologie (Celle) 2010; 41: 99-108
  • 56 Vasquez A, Forsgren E, Fries I, Paxton RJ, Flaberg E, Szekely L, Olofsson TC. Symbionts as major modulators of insect health: lactic acid bacteria and honeybees. PLoS One 2012; 7: e33188
  • 57 Evans JD, Schwarz RS. Bees brought to their knees: microbes affecting honey bee health. Trends Microbiol 2011; 19: 614-620
  • 58 White GF. Bacteria of the apiary. Technical series (United States Bureau of Entomology) 1906; 14 DOI: 10.5962/bhl.title.87503.
  • 59 Ashiralieva A, Genersch E. Reclassification, genotypes and virulence of Paenibacillus larvae, the etiological agent of American foulbrood in honeybees–a review. Apidologie (Celle) 2006; 37: 411-420
  • 60 Crailsheim K, Riessberger-Gallé U. Honey bee age-dependent resistance against American foulbrood. Apidologie (Celle) 2001; 32: 91-103
  • 61 Genersch E. American foulbrood in honeybees and its causative agent, Paenibacillus larvae . J Invertebr Pathol 2010; 103: S10-S19
  • 62 Waite R, Brown M, Thompson H, Bew M. Control of American foulbrood by eradication of infected colonies. Apiacta 2003; 38: 134-136
  • 63 Reybroeck W, Daeseleire E, De Brabander HF, Herman L. Antimicrobials in beekeeping. Vet Microbiol 2012; 158: 1-11
  • 64 Alippi AM, Albo GN, Leniz D, Rivera I, Zanelli ML, Roca AE. Comparative study of tylosin, erythromycin and oxytetracycline to control American foulbrood of honey bees. J Apicult Res 1999; 38: 149-158
  • 65 Kochansky J, Knox DA, Feldlaufer M, Pettis JS. Screening alternative antibiotics against oxytetracycline-susceptible and-resistant Paenibacillus larvae . Apidologie (Celle) 2001; 32: 215-222
  • 66 Katznelson H. The influence of antibiotics and sulfa drugs on Bacillus larvae, cause of American foulbrood of the honeybee, in vitro and in vivo . J Bacteriol 1950; 59: 471
  • 67 Kochansky J, Pettis J. Screening additional antibiotics for efficacy against American foulbrood. J Apicult Res 2005; 44: 24-28
  • 68 Bogdanov S. Contaminants of bee products. Apidologie (Celle) 2006; 37: 1-18
  • 69 Funfhaus A, Ebeling J, Genersch E. Bacterial pathogens of bees. Curr Opin Insect Sci 2018; 26: 89-96
  • 70 Koch H, Schmid-Hempel P. Socially transmitted gut microbiota protect bumble bees against an intestinal parasite. P Natl Acad Sci USA 2011; 108: 19288-19292
  • 71 Michener CD. The Meliponini. In: Pot-honey: a legacy of stingless bees. Springer; 2013: 3-17
  • 72 Whitfield CW, Behura SK, Berlocher SH, Clark AG, Johnston JS, Sheppard WS, Smith DR, Suarez AV, Weaver D, Tsutsui ND. Thrice out of Africa: ancient and recent expansions of the honey bee, Apis mellifera . Science 2006; 314: 642-645
  • 73 Purkiss T, Lach L. Pathogen spillover from Apis mellifera to a stingless bee. P Roy Soc B-Biol Sci 2019; 286: 20191071
  • 74 Shanks JL, Haigh AM, Riegler M, Spooner-Hart RN. First confirmed report of a bacterial brood disease in stingless bees. J Invertebr Pathol 2017; 144: 7-10
  • 75 Ueira-Vieira C, Almeida LO, de Almeida FC, Amaral IMR, Brandeburgo MAM, Bonetti AM. Scientific note on the first molecular detection of the acute bee paralysis virus in Brazilian stingless bees. Apidologie (Celle) 2015; 46: 628-630
  • 76 Teixeira EW, Ferreira EA, da Luz CFP, Martins MF, Ramos TA, Lourenco AP. European foulbrood in stingless bees (Apidae: Meliponini) in Brazil: old disease, renewed threat. J Invertebr Pathol 2020; 172: 107357
  • 77 Olofsson TC, Butler E, Markowicz P, Lindholm C, Larsson L, Vasquez A. Lactic acid bacterial symbionts in honeybees–an unknown key to honeyʼs antimicrobial and therapeutic activities. Int Wound J 2016; 13: 668-679
  • 78 Leonhardt SD, Kaltenpoth M. Microbial communities of three sympatric Australian stingless bee species. PLoS One 2014; 9: e105718
  • 79 Audisio MC, Torres MJ, Sabate DC, Ibarguren C, Apella MC. Properties of different lactic acid bacteria isolated from Apis mellifera L. bee-gut. Microbiol Res 2011; 166: 1-13
  • 80 Cambronero-Heinrichs JC, Matarrita-Carranza B, Murillo-Cruz C, Araya-Valverde E, Chavarria M, Pinto-Tomas AA. Phylogenetic analyses of antibiotic-producing Streptomyces sp. isolates obtained from the stingless-bee Tetragonisca angustula (Apidae: Meliponini). Microbiol-Sgm 2019; 165: 292-301
  • 81 Promnuan Y, Kudo T, Chantawannakul P. Actinomycetes isolated from beehives in Thailand. World J Microb Biot 2009; 25: 1685-1689
  • 82 Menezes C, Vollet-Neto A, Marsaioli AJ, Zampieri D, Fontoura IC, Luchessi AD, Imperatriz-Fonseca VL. A Brazilian social bee must cultivate fungus to survive. Curr Biol 2015; 25: 2851-2855
  • 83 Paludo CR, Menezes C, Silva-Junior EA, Vollet-Neto A, Andrade-Dominguez A, Pishchany G, Khadempour L, Nascimento FS, Currie CR, Kolter R, Clardy J, Pupo MT. Stingless bee larvae require fungal steroid to pupate. Sci Rep 2018; 8: 1122
  • 84 Paludo CR, Pishchany G, Andrade-Dominguez A, Silva-Junior EA, Menezes C, Nascimento FS, Currie CR, Kolter R, Clardy J, Pupo MT. Microbial community modulates growth of symbiotic fungus required for stingless bee metamorphosis. PLoS One 2019; 14: e0219696
  • 85 Barbosa R, Leong S, Vinnere-Pettersson O, Chen A, Souza-Motta C, Frisvad J, Samson R, Oliveira N, Houbraken J. Phylogenetic analysis of Monascus and new species from honey, pollen and nests of stingless bees. Stud Mycol 2017; 86: 29-51
  • 86 Paludo CR, Ruzzini AC, Silva-Junior EA, Pishchany G, Currie CR, Nascimento FS, Kolter RG, Clardy J, Pupo MT. Whole-genome sequence of Bacillus sp. SDLI1, isolated from the social bee Scaptotrigona depilis . Genome Announc 2016; 4: e00174-00116
  • 87 Evans JD, Armstrong TN. Inhibition of the American foulbrood bacterium, Paenibacillus larvae larvae, by bacteria isolated from honey bees. J Apicult Res 2005; 44: 168-171
  • 88 Gilliam M. Identification and roles of non-pathogenic microflora associated with honey bees. FEMS Microbiol Lett 1997; 155: 1-10
  • 89 Cano RJ, Borucki MK, Higbyschweitzer M, Poinar HN, Poinar GO, Pollard KJ. Bacillus dna in fossil bees–an ancient symbiosis. Appl Environ Microb 1994; 60: 2164-2167
  • 90 Menegatti C, Melo WGP, Carrão DB, Oliveira ARM, Nascimento FS, Lopes NP, Pupo MT. Paenibacillus polymyxa associated with the stingless bee Melipona scutellaris produces antimicrobial compounds against entomopathogens. J Chem Ecol 2018; 44: 1158-1169
  • 91 Rodriguez-Hernandez D, Melo WGP, Menegatti C, Lourenzon VB, Nascimento FS, Pupo MT. Actinobacteria associated with stingless bee biosynthesize bioactive polyketides against bacterial pathogen. New J Chem 2019; 43: 10109-10117
  • 92 Menegatti C, Lourenzon VB, Rodríguez-Hernández D, Melo WGP, Ferreira LLG, Andricopulo AD, Nascimento FS, Pupo MT. Meliponamycins: antimicrobials from stingless bee-associated Streptomyces sp. J Nat Prod 2020; 83: 610-616
  • 93 Kaltenpoth M, Goettler W, Dale C, Stubblefield JW, Herzner G, Roeser-Mueller K, Strohm E. “Candidatus Streptomyces philanthi”, an endosymbiotic streptomycete in the antennae of Philanthus digger wasps. Int J Syst Evol Micr 2006; 56: 1403-1411
  • 94 Bohart RM, Bohart RM, Menke AS. Sphecid Wasps of the World: A Generic Revision. Berkeley: University of California Press; 1976
  • 95 Kaltenpoth M, Goettler W, Koehler S, Strohm E. Life cycle and population dynamics of a protective insect symbiont reveal severe bottlenecks during vertical transmission. Evol Ecol 2010; 24: 463-477
  • 96 Kroiss J, Kaltenpoth M, Schneider B, Schwinger MG, Hertweck C, Maddula RK, Strohm E, Svatos A. Symbiotic streptomycetes provide antibiotic combination prophylaxis for wasp offspring. Nat Chem Biol 2010; 6: 261-263
  • 97 Kaltenpoth M, Schmitt T, Polidori C, Koedam D, Strohm E. Symbiotic streptomycetes in antennal glands of the South American digger wasp genus Trachypus (Hymenoptera, Crabronidae). Physiol Entomol 2010; 35: 196-200
  • 98 Douglas AE. Lessons from studying insect symbioses. Cell Host Microbe 2011; 10: 359-367
  • 99 Dedeine F, Vavre F, Fleury F, Loppin B, Hochberg ME, Bouletreau M. Removing symbiotic Wolbachia bacteria specifically inhibits oogenesis in a parasitic wasp. P Natl Acad Sci USA 2001; 98: 6247-6252
  • 100 Kremer N, Charif D, Henri H, Gavory F, Wincker P, Mavingui P, Vavre F. Influence of Wolbachia on host gene expression in an obligatory symbiosis. BMC Microbiol 2012; 12: S7
  • 101 Zchori-Fein E, Gottlieb Y, Kelly SE, Brown JK, Wilson JM, Karr TL, Hunter MS. A newly discovered bacterium associated with parthenogenesis and a change in host selection behavior in parasitoid wasps. P Natl Acad Sci USA 2001; 98: 12555-12560
  • 102 Zchori-Fein E, Perlman SJ, Kelly SE, Katzir N, Hunter MS. Characterization of a ‘bacteroidetes’ symbiont in Encarsia wasps (Hymenoptera: Aphelinidae): proposal of ‘Candidatus Cardinium hertigii’ . Int J Syst Evol Micr 2004; 54: 961-968
  • 103 Chan MS, Godfray HCJ. Host-feeding strategies of parasitoid wasps. Evol Ecol 1993; 7: 593-604
  • 104 Roossinck MJ. The good viruses: viral mutualistic symbioses. Nat Rev Microbiol 2011; 9: 99-108
  • 105 Villarreal LP. Virus-host symbiosis mediated by persistence. Symbiosis 2007; 44: 1-9
  • 106 Yamamura N. Evolution of mutualistic symbiosis: a differential equation model. Res Popul Ecol 1996; 38: 211-218
  • 107 Whitfield JB. Estimating the age of the polydnavirus/braconid wasp symbiosis. P Natl Acad Sci USA 2002; 99: 7508-7513
  • 108 Adams AS, Jordan MS, Adams SM, Suen G, Goodwin LA, Davenport KW, Currie CR, Raffa KF. Cellulose-degrading bacteria associated with the invasive woodwasp Sirex noctilio . ISME J 2011; 5: 1323-1331
  • 109 Kukor JJ, Martin MM. Acquisition of digestive enzymes by siricid woodwasps from their fungal symbiont. Science 1983; 220: 1161-1163
  • 110 Somavilla A, de Oliveira ML, Silveira OT. Diversity and aspects of the ecology of social wasps (Vespidae, Polistinae) in central Amazonian “terra firme” forest. Rev Bras Entomol 2014; 58: 349-355
  • 111 Adnani N, Rajski SR, Bugni TS. Symbiosis-inspired approaches to antibiotic discovery. Nat Prod Rep 2017; 34: 784-814
  • 112 Mueller UG, Gerardo N. Fungus-farming insects: multiple origins and diverse evolutionary histories. P Natl Acad Sci 2002; 99: 15247-15249
  • 113 Aanen DK, Eggleton P, Rouland-Lefevre C, Guldberg-Froslev T, Rosendahl S, Boomsma JJ. The evolution of fungus-growing termites and their mutualistic fungal symbionts. P Natl Acad Sci USA 2002; 99: 14887-14892
  • 114 Kambhampati S, Eggleton P. Taxonomy and Phylogeny of Termites. In: Abe T, Bignell DE, Higashi M. eds. Termites: Evolution, Sociality, Symbioses, Ecology. Dordrecht: Kluwer Academic Publishers; 2000: 1-23
  • 115 Lima JT, Costa-Leonardo AM. Recursos alimentares explorados pelos cupins (Insecta: Isoptera). Biota Neotrop 2007; bn04007022007
  • 116 Grieco MB, Lopes FAC, Oliveira LS, Tschoeke DA, Popov CC, Thompson CC, Goncalves LC, Constantino R, Martins OB, Kruger RH, de Souza W, Thompson FL. Metagenomic analysis of the whole gut microbiota in Brazilian termitidae termites Cornitermes cumulans, Cyrilliotermes strictinasus, Syntermes dirus, Nasutitermes jaraguae, Nasutitermes aquilinus, Grigiotermes bequaerti, and Orthognathotermes mirim . Curr Microbiol 2019; 76: 687-697
  • 117 Padilla MA, Rodrigues RAF, Bastos JCS, Martini MC, Barnabe ACD, Kohn LK, Uetanabaro APT, Bomfim GF, Afonso RS, Fantinatti-Garboggini F, Arns CW. Actinobacteria from termite mounds show antiviral activity against bovine viral diarrhea virus, a surrogate model for hepatitis c virus. Evid-Based Compl Alt 2015; 1-9
  • 118 Wyche TP, Ruzzini AC, Beemelmanns C, Kim KH, Klassen JL, Cao S, Poulsen M, Bugni TS, Currie CR, Clardy J. Linear peptides are the major products of a biosynthetic pathway that encodes for cyclic depsipeptides. Org Lett 2017; 19: 1772-1775
  • 119 Benndorf R, Guo H, Sommerwerk E, Weigel C, Garcia-Altares M, Martin K, Hu H, Küfner M, De Beer ZW, Poulsen M. Natural products from actinobacteria associated with fungus-growing termites. Antibiotics 2018; 7: 83
  • 120 Klassen JL, Lee SR, Thomas-Poulsen M, Beemelmanns C, Kim KH. Efomycins K and L from a termite-associated Streptomyces sp. m56 and their putative biosynthetic origin. Front Microbiol 2019; 10: 1739
  • 121 Lee SR, Song JH, Song JH, Ko HJ, Baek JY, Trinh TA, Beemelmanns C, Yamabe N, Kim KH. Chemical identification of isoflavonoids from a termite-associated Streptomyces sp. RB1 and their neuroprotective effects in murine hippocampal HT22 cell line. Int J Mol Sci 2018; 19: 2640
  • 122 Lee SR, Lee D, Yu JS, Benndorf R, Lee S, Lee DS, Huh J, De Beer ZW, Kim YH, Beemelmanns C. Natalenamides A–C, cyclic tripeptides from the termite-associated Actinomadura sp. RB99. Molecules 2018; 23: 3003
  • 123 Beemelmanns C, Ramadhar TR, Kim KH, Klassen JL, Cao S, Wyche TP, Hou Y, Poulsen M, Bugni TS, Currie CR. Macrotermycins A–D, glycosylated macrolactams from a termite-associated Amycolatopsis sp. M39. Org Lett 2017; 19: 1000-1003
  • 124 Yoon SY, Lee SR, Hwang JY, Benndorf R, Beemelmanns C, Chung SJ, Kim KH. Fridamycin A, a microbial natural product, stimulates glucose uptake without inducing adipogenesis. Nutrients 2019; 11: 765
  • 125 Carr G, Poulsen M, Klassen JL, Hou Y, Wyche TP, Bugni TS, Currie CR, Clardy J. Microtermolides A and B from termite-associated Streptomyces sp. and structural revision of vinylamycin. Org Lett 2012; 14: 2822-2825
  • 126 Yang Z, Ma M, Yang CH, Gao Y, Zhang Q, Chen Y. Determination of the absolute configurations of microtermolides A and B. J Nat Prod 2016; 79: 2408-2412
  • 127 Constantino R, Acioli A. Termite diversity in Brazil (Insecta: Isoptera). In: Moreira FMS, Siqueira JO. editors Soil biodiversity in Amazonian and other Brazilian ecosystems. Wallingforg: CAB International; 2006: 117-128
  • 128 Hernandez ILC, Godinho MJL, Magalhaes A, Schefer AB, Ferreira AG, Berlinck RGS. N-acetyl-gamma-hydroxyvaline lactone, an unusual amino acid derivative from marine streptomycete. J Nat Prod 2000; 63: 664-665
  • 129 Chagas FO, Dias LG, Pupo MT. A mixed culture of endophytic fungi increases production of antifungal polyketides. J Chem Ecol 2013; 39: 1335-1342
  • 130 Sanchez-Bayo F, Wyckhuys KAG. Worldwide decline of the entomofauna: a review of its drivers. Biol Conserv 2019; 232: 8-27