Abstract
Actinobacteria are Gram-positive bacteria, which have been known for their roles in various fields in human life, especially in medicine. They constitute a highly diverse phylum with an unrivalled metabolic versatility. Finding novel antibiotics is highly important since drug-resistant infections are a serious threat to people's health. Since Actinobacteria, especially those from the genus Streptomyces, have been known as prolific producers of antibiotics, isolating rare or novel actinobacterial species from uncommon habitats like the ones associated with insects and mollusks might increase the chance to discover novel active compounds. Numerous actinobacterial strains have been isolated from insects (ants, termites, bees, wasps, beetles, and bugs) and mollusks (nudibranchs, snails, and clams) with different genera and bioactive properties. Moreover, rare Actinobacteria like Actinocorallia, Verrucosispora, Sphaerisporangium, Actinocatenispora, Agromyces, and Saccharothrix were isolated from these invertebrates. Various active compounds such as furamycins, anthracyclines, lobophorins, antimycins, julichromes, nocapyrones, pulicatins, and saccharothrixmicines examplify that insects and mollusks represent valuable sources for interesting secondary metabolites.
This is a preview of subscription content, log in via an institution to check access.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Abdelrahman SM, Patin NV, Hanora A, Aboseidah A, Desoky S, Desoky SG, Stewart FJ, Lopanik NB (2021) The natural product biosynthetic potential of Red Sea nudibranch microbiomes. PeerJ 9:1–26. https://doi.org/10.7717/peerj.10525
Adams AS, Jordan MS, Adams SM, Suen G, Goodwin LA, Davenport KW, Currie CR, Raffa KF (2011) Cellulose-degrading bacteria associated with the invasive woodwasp Sirex noctilio. ISME J 5(8):1323–1331. https://doi.org/10.1038/ismej.2011.14
Bae M, Yamada K, Ijuin Y, Tsuji T, Yazawa K, Uemura D (1996) Aburatubolactam A, a novel inhibitor of superoxide anion generation from a marine microorganism. Heterocycl Commun 2(4):315–318. https://doi.org/10.1515/HC.1996.2.4.315
Barka EA, Vatsa P, Sanchez L, Gaveau-Vaillant N, Jacquard C, Klenk H-P, Clément C, Ouhdouch Y, van Wezel GP (2016) Taxonomy, physiology, and natural products of Actinobacteria. Microbiol Mol Biol Rev 80(1):1–43. https://doi.org/10.1128/MMBR.00019-15
Beemelmanns C, Ramadhar TR, Kim KH, Klassen JL, Cao S, Wyche TP, Hou Y, Poulsen M, Bugni TS, Currie CR, Clardy J (2017) Macrotermycins A-D, glycosylated macrolactams from a termite-associated Amycolatopsis sp. M39. Org Lett 19(5):1000–1003. https://doi.org/10.1021/acs.orglett.6b03831
Benkendorff K (2010) Molluscan biological and chemical diversity: secondary metabolites and medicinal resources produced by marine molluscs. Biol Rev 85(4):757–775
Benndorf R, Guo H, Sommerwerk E, Weigel C, Garcia-Altares M, Martin K, Hu H, Küfner M, de Beer ZW, Poulsen M, Beemelmanns C (2018) Natural products from Actinobacteria associated with fungus-growing termites. Antibiotics 7(3):1–25. https://doi.org/10.3390/antibiotics7030083
Bewley CA, Holland ND, Faulkner DJ (1996) Two classes of metabolites from Theonella swinhoei are localized in distinct populations of bacterial symbionts. Experientia 52(7):716–722. https://doi.org/10.1007/BF01925581
Brusca RC, Brusca GJ (2003) Invertebrates. Basingstoke
Cafaro MJ, Currie CR (2005) Phylogenetic analysis of mutualistic filamentous bacteria associated with fungus-growing ants. Can J Microbiol 51(6):441–446. https://doi.org/10.1139/w05-023
Caffrey P, Lynch S, Flood E, Finnan S, Oliynyk M (2001) Amphotericin biosynthesis in Streptomyces nodosus: deductions from analysis of polyketide synthase and late genes. Chem Biol 8(7):713–723. https://doi.org/10.1016/S1074-5521(01)00046-1
Cambronero-Heinrichs JC, Matarrita-Carranza B, Murillo-Cruz C, Araya-Valverde E, Chavarría M, Pinto-Tomás AA (2019) Phylogenetic analyses of antibiotic-producing Streptomyces sp. isolates obtained from the stingless-bee Tetragonisca angustula (Apidae: Meliponini). Microbiology (United Kingdom) 165(3):292–301. https://doi.org/10.1099/mic.0.000754
Cazemier AE, Verdoes JC, Reubsaet FAG, Hackstein JHP, van der Drift C, Op den Camp HJM (2003) Promicromonospora pachnodae sp. nov., a member of the (hemi)cellulolytic hindgut flora of larvae of the scarab beetle Pachnoda marginata. Antonie Van Leeuwenhoek 83(2):135–148. https://doi.org/10.1023/A:1023325817663
Currie CR, Scottt JA, Summerbell RC, Malloch D (1999) Fungus-growing ants use antibiotic-producing bacteria to control garden parasites. Nature 398(6729):701–704. https://doi.org/10.1038/19519
de Lima Procópio RE, da Silva IR, Martins MK, de Azevedo JL, de Araújo JM (2012) Antibiotics produced by Streptomyces. Braz J Infect Dis 16(5):466–471. https://doi.org/10.1016/j.bjid.2012.08.014
Defossez E, Selosse M-A, Dubois M-P, Mondolot L, Faccio A, Djieto-Lordon C, McKey D, Blatrix R (2009) Ant-plants and fungi: a new threeway symbiosis. New Phytol 182(4):942–949. https://doi.org/10.1111/j.1469-8137.2009.02793.x
Dejean A, Solano PJ, Ayroles J, Corbara B, Orivel J (2005) Arboreal ants build traps to capture prey. Nature 434(7036):973–973. https://doi.org/10.1038/434973a
Dong Y, Ding W, Sun C, Ji X, Ling C, Zhou Z, Chen Z, Chen X, Ju J (2020) Julichrome Monomers from marine gastropod mollusk-associated Streptomyces and stereochemical revision of julichromes Q3 · 5 and Q3 · 3. Chem Biodivers 17(4):e2000057
El-Shatoury SA, El-Shenawy NS, Abd El-Salam IM (2009) Antimicrobial, antitumor and in vivo cytotoxicity of actinomycetes inhabiting marine shellfish. World J Microbiol Biotechnol 25(9):1547–1555
Grubbs KJ, Surup F, Biedermann PHW, McDonald BR, Klassen JL, Carlson CM, Clardy J, Currie CR (2020) Cycloheximide-producing Streptomyces associated with Xyleborinus saxesenii and Xyleborus affinis fungus-farming ambrosia beetles. Front Microbiol 11:1–12. https://doi.org/10.3389/fmicb.2020.562140
Heil M, McKey D (2003) Protective ant-plant interactions as model systems in ecological and evolutionary research. Annu Rev Ecol Evol Syst 34(1):425–553. https://doi.org/10.1146/annurev.ecolsys.34.011802.132410
Henderson JA, Phillips AJ (2008) Total synthesis of aburatubolactam A. Angew Chem Int Ed Engl 47(44):8499–8501. https://doi.org/10.1002/anie.200803593
Herbert DG, Hamer ML, Mander M, Mkhize N, Prins F (2003) Invertebrate animals as a component of the traditional medicine trade in KwaZulu-Natal, South Africa. Afr Invertebr 44(2):1–8
Hoshino Y, Mukai A, Yazawa K, Uno J, Ishikawa J, Ando A, Fukai T, Mikami Y (2004) Transvalencin A, a thiazolidine zinc complex antibiotic produced by a clinical isolate of Nocardia transvalensis: I. Taxonomy, fermentation, isolation and biological activities. J Antibiot (Tokyo) 57(12):797–802. https://doi.org/10.7164/antibiotics.57.797
Hu SY, Kong YC, But PP (1999) An enumeration of Chinese materia medica. Chinese University Press
Hu Z, Chen X, Chang J, Yu J, Tong Q, Li S, Niu H (2018) Compositional and predicted functional analysis of the gut microbiota of Radix auricularia (Linnaeus) via high-throughput Illumina sequencing. PeerJ 6:e5537
Hulcr J, Adams AS, Raffa K, Hofstetter RW, Klepzig KD, Currie CR (2011) Presence and diversity of Streptomyces in Dendroctonus and sympatric bark beetle galleries across North America. Microb Ecol 61(4):759–768. https://doi.org/10.1007/s00248-010-9797-0
Jelić D, Antolović R (2016) From erythromycin to azithromycin and new potential ribosome-binding antimicrobials. Antibiotics 5(3):29. https://doi.org/10.3390/antibiotics5030029
Ji X, Dong Y, Ling C, Zhou Z, Li Q, Ju J (2020) Elucidation of the tailoring steps in julichrome biosynthesis by marine gastropod mollusk-associated Streptomyces sampsonii SCSIO 054. Org Lett 22(17):6927–6931
Joynson R, Pritchard L, Osemwekha E, Ferry N (2017) Metagenomic analysis of the gut microbiome of the common black slug Arion ater in search of novel lignocellulose degrading enzymes. Front Microbiol 8:2181
Kalinovskaya NI, Kalinovsky AI, Romanenko LA, Dmitrenok PS, Kuznetsova TA (2010) New angucyclines and antimicrobial diketopiperazines from the marine mollusk-derived actinomycete Saccharothrix espanaensis An 113. Nat Prod Commun 5(4):597–602
Kaltenpoth M, Goettler W, Dale C, Stubblefield JW, Herzner G, Roeser-Mueller K, Strohm E (2006) “Candidatus Streptomyces philanthi”, an endosymbiotic streptomycete in the antennae of Philanthus digger wasps. Int J Syst Evol Microbiol 56(6):1403–1411. https://doi.org/10.1099/ijs.0.64117-0
Kaltenpoth M, Schmitt T, Polidori C, Koedam D, Strohm E (2010) Symbiotic streptomycetes in antennal glands of the South American digger wasp genus Trachypus (Hymenoptera, Crabronidae). Physiol Entomol 35(2):196–200. https://doi.org/10.1111/j.1365-3032.2010.00729.x
Karuppiah V, Sun W, Li Z (2016) Natural products of Actinobacteria derived from marine organisms. In: Studies in natural products chemistry, vol 48. Elsevier, pp 417–446
Kharel MK, Pahari P, Shepherd MD, Tibrewal N, Nybo SE, Shaaban KA, Rohr J (2012) Angucyclines: biosynthesis, mode-of-action, new natural products, and synthesis. Nat Prod Rep 29(2):264–325
Kim HJ, Han CY, Park JS, Oh SH, Kang SH, Choi SS, Kim JM, Kwak JH, Kim ES (2018) Nystatin-like Pseudonocardia polyene B1, a novel disaccharide-containing antifungal heptaene antibiotic. Sci Rep 8(1):1–8. https://doi.org/10.1038/s41598-018-31801-y
King GM, Judd C, Kuske CR, Smith C (2012) Analysis of stomach and gut microbiomes of the eastern oyster (Crassostrea virginica) from coastal Louisiana, USA. PLoS One 7(12):e51475
Kocot KM, Cannon JT, Todt C, Citarella MR, Kohn AB, Meyer A, Santos SR, Schander C, Moroz LL, Lieb B, Halanych KM (2011) Phylogenomics reveals deep molluscan relationships. Nature 477(7365):452–456. https://doi.org/10.1038/nature10382
Li LH, Lv S, Lu Y, Bi DQ, Guo YH, Wu JT, Yue ZY, Mao GY, Guo ZX, Zhang Y, Tang YF (2019) Spatial structure of the microbiome in the gut of Pomacea canaliculata. BMC Microbiol 19(1):1–9
Lin Z, Antemano RR, Hughen RW, Tianero MD, Peraud O, Haygood MG, Concepcion GP, Olivera BM, Light A, Schmidt EW (2010) Pulicatins A-E, neuroactive thiazoline metabolites from cone snail-associated bacteria. J Nat Prod 73(11):1922–1926
Lin Z, Reilly CA, Antemano R, Hughen RW, Marett L, Concepcion GP, Haygood MG, Olivera BM, Light A, Schmidt EW (2011) Nobilamides A-H, long-acting transient receptor potential vanilloid-1 (TRPV1) antagonists from mollusk-associated bacteria. J Med Chem 54(11):3746–3755
Lin Z, Flores M, Forteza I, Henriksen NM, Concepcion GP, Rosenberg G, Haygood MG, Olivera BM, Light AR, Cheatham TE III, Schmidt EW (2012) Totopotensamides, polyketide-cyclic peptide hybrids from a mollusk-associated bacterium Streptomyces sp. J Nat Prod 75(4):644–649
Lin Z, Marett L, Hughen RW, Flores M, Forteza I, Ammon MA, Concepcion GP, Espino S, Olivera BM, Rosenberg G, Haygood MG, Light AR, Schmidt EW (2013a) Neuroactive diol and acyloin metabolites from cone snail-associated bacteria. Bioorg Med Chem Lett 23(17):4867–4869. https://doi.org/10.1016/j.bmcl.2013.06.088
Lin Z, Torres JP, Ammon MA, Marett L, Teichert RW, Reilly CA, Kwan JC, Hughen RW, Flores M, Tianero MD, Peraud O (2013b) A bacterial source for mollusk pyrone polyketides. Chem Biol 20(1):73–81. https://doi.org/10.1016/j.chembiol.2012.10.019
Luesch H, Moore RE, Paul VJ, Mooberry SL, Corbett TH (2001) Isolation of dolastatin 10 from the marine cyanobacterium Symploca species VP642 and total stereochemistry and biological evaluation of its analogue symplostatin 1. J Nat Prod 64(7):907–910
Luypaert T, Hagan JG, McCarthy ML, Poti M (2020) Status of marine biodiversity in the anthropocene. In: Jungblut S, Liebich V, Bode-Dalby M (eds) YOUMARES 9—the oceans: our research, our future. Springer, Cham. https://doi.org/10.1007/978-3-030-20389-4_4
Mandala SM, Thornton RA, Milligan J, Rosenbach M, Garcia-Calvo M, Bull HG, Harris G, Abruzzo GK, Flattery AM, Gill CJ, Bartizal K, Dreikorn S, Kurtz MB (1998) Rustmicin, a potent antifungal agent, inhibits sphingolipid synthesis at inositol phosphoceramide synthase. J Biol Chem 273(24):14942–14949. https://doi.org/10.1074/jbc.273.24.14942
Matarrita-Carranza B, Moreira-Soto RD, Murillo-Cruz C, Mora M, Currie CR, Pinto-Tomas AA (2017) Evidence for widespread associations between neotropical hymenopteran insects and Actinobacteria. Front Microbiol 8:1–17. https://doi.org/10.3389/fmicb.2017.02016
Matarrita-Carranza B, Murillo-Cruz C, Avendaño R, Ríos MI, Chavarría M, Gómez-Calvo ML, Tamayo-Castillo G, Araya JJ, Pinto-Tomás AA (2021) Streptomyces sp. M54: an actinobacteria associated with a neotropical social wasp with high potential for antibiotic production. Antonie Van Leeuwenhoek 114:379–398. https://doi.org/10.1007/s10482-021-01520-y
McGuire JM, Bunch RL, Anderson RC, Boaz HE, Flynn EH, Powell HM, Smith JW (1952) Ilotycin, a new antibiotic. Antibiot Chemother (Northfield) 2(6):281–283
Mioduchowska M, Zając K, Bartoszek K, Madanecki P, Kur J, Zając T (2020) 16S rRNA gene-based metagenomic analysis of the gut microbial community associated with the DUI species Unio crassus (Bivalvia: Unionidae). J Zool Syst Evol Res 58(2):615–623
Mogouong J, Constant P, Lavallée R, Guertin C (2020) Gut microbiome of the emerald ash borer, Agrilus planipennis Fairmaire, and its relationship with insect population density. FEMS Microbiol Ecol 96(8):1–12. https://doi.org/10.1093/femsec/fiaa141
Mohr KI, Tebbe CC (2006) Diversity and phylotype consistency of bacteria in the guts of three bee species (Apoidea) at an oilseed rape field. Environ Microbiol 8(2):258–272. https://doi.org/10.1111/j.1462-2920.2005.00893.x
Müller R, Wink J (2014) Future potential for anti-infectives from bacteria—how to exploit biodiversity and genomic potential. Int J Med Microbiol 304(1):3–13. https://doi.org/10.1016/j.ijmm.2013.09.004
Nielsen RV, Hyldig-Nielsen F, Jacobsen K (1982) Biological properties of ristocetin-Ψ-aglycone. J Antibiot (Tokyo) 35(11):1561–1564. https://doi.org/10.7164/antibiotics.35.1561
Parkhaev PY (2017) Origin and the early evolution of the phylum Mollusca. Paleontol J 51(6):663–686
Pasti MB, Belli ML (1985) Cellulolytic activity of actinomycetes isolated from termites (Termitidae) gut. FEMS Microbiol Lett 26(1):107–112. https://doi.org/10.1111/j.1574-6968.1985.tb01574.x
Pati P, Sahu BK, Panigrahy RC (2015) Marine molluscs as a potential drug cabinet: an overview. Indian J Geo-Mar Sci 44(7):961–970
Peraud O, Biggs JS, Hughen RW, Light AR, Concepcion GP, Olivera BM, Schmidt EW (2009) Microhabitats within venomous cone snails contain diverse actinobacteria. Appl Environ Microbiol 75(21):6820–6826. https://doi.org/10.1128/AEM.01238-09
Pinheiro GL, Correa R, Soares R, Cardoso A, Chaia C, Clementino MM, Garcia E, De Souza W, Frasés S (2015) Isolation of aerobic cultivable cellulolytic bacteria from different regions of the gastrointestinal tract of giant land snail Achatina fulica. Front Microbiol 6:860
Poulsen M, Oh DC, Clardy J, Currie CR (2011) Chemical analyses of wasp-associated Streptomyces bacteria reveal a prolific potential for natural products discovery. PLoS One 6(2):e16763. https://doi.org/10.1371/journal.pone.0016763
Prommer E (2006) Ziconotide: a new option for refractory pain. Drugs Today 42(6):369–378
Risdian C, Mozef T, Wink J (2019) Biosynthesis of polyketides in Streptomyces. Microorganisms 7(5):124
Riyanti R, Widada J, Radjasa OK (2009) Isolation and screening of antimicrobial producing-actinomycetes symbionts in nudibranch. Indones J Biotechnol 14:1132–1138. https://doi.org/10.22146/ijbiotech.7807
Rodríguez-Hernández D, Melo WGP, Menegatti C, Lourenzon VB, do Nascimento FS, Pupo MT (2019) Actinobacteria associated with stingless bees biosynthesize bioactive polyketides against bacterial pathogens. New J Chem 43(25):10109–10117. https://doi.org/10.1039/C9NJ01619H
Romanenko LA, Uchino M, Kalinovskaya NI, Mikhailov VV (2008) Isolation, phylogenetic analysis and screening of marine mollusc-associated bacteria for antimicrobial, hemolytic and surface activities. Microbiol Res 163(6):633–644. https://doi.org/10.1016/j.micres.2006.10.001
Ruiz-González MX, Malé PJG, Leroy C, Dejean A, Gryta H, Jargeat P, Quilichini A, Orivel J (2011) Specific, non-nutritional association between an ascomycete fungus and Allomerus plant-ants. Biol Lett 7(3):475–479. https://doi.org/10.1098/rsbl.2010.0920
Ruppert EE, Barnes RD (1994) Invertebrate zoology. Saunders College Publishing, Fort Worth
Safaei N, Mast Y, Steinert M, Huber K, Bunk B, Wink J (2021) Angucycline-like aromatic polyketide from a novel Streptomyces species reveals freshwater snail Physa acuta as underexplored reservoir for antibiotic-producing actinomycetes. Antibiotics 10(1):22
Salem H, Kreutzer E, Sudakaran S, Kaltenpoth M (2013) Actinobacteria as essential symbionts in firebugs and cotton stainers (Hemiptera, Pyrrhocoridae). Environ Microbiol 15(7):1956–1968. https://doi.org/10.1111/1462-2920.12001
Schneemann I, Ohlendorf B, Zinecker H, Nagel K, Wiese J, Imhoff JF (2010) Nocapyrones A-D, γ-pyrones from a Nocardiopsis strain isolated from the marine sponge Halichondria panicea. J Nat Prod 73(8):1444–1447
Seipke RF, Barke J, Ruiz-Gonzalez MX, Orivel J, Yu DW, Hutchings MI (2012a) Fungus-growing Allomerus ants are associated with antibiotic-producing actinobacteria. Antonie Van Leeuwenhoek 101(2):443–447. https://doi.org/10.1007/s10482-011-9621-y
Seipke RF, Kaltenpoth M, Hutchings MI (2012b) Streptomyces as symbionts: an emerging and widespread theme? FEMS Microbiol Rev 36(4):862–876. https://doi.org/10.1111/j.1574-6976.2011.00313.x
Takacs-Vesbach C, King K, Van Horn D, Larkin K, Neiman M (2016) Distinct bacterial microbiomes in sexual and asexual Potamopyrgus antipodarum, a New Zealand freshwater snail. PLoS One 11(8):e0161050
Takatsu T, Nakayama H, Shimazu A, Furihata K, Ikeda K, Furihata K, Seto H, Otake N (1985) Rustmicin, a new macrolide antibiotic active against wheat stem rust fungus. J Antibiot (Tokyo) 38(12):1806–1809
Visser AA, Nobre T, Currie CR, Aanen DK, Poulsen M (2012) Exploring the potential for actinobacteria as defensive symbionts in fungus-growing termites. Microb Ecol 63(4):975–985. https://doi.org/10.1007/s00248-011-9987-4
Waksman SA, Reilly HC, Johnstone DB (1946) Isolation of streptomycin-producing strains of Streptomyces griseus. J Bacteriol 52(3):393–397. https://jb.asm.org/content/52/3/393.long
Wang Z, Yu Z, Zhao J, Zhuang X, Cao P, Guo X, Liu C, Xiang W (2020) Community composition, antifungal activity and chemical analyses of ant-derived actinobacteria. Front Microbiol 11:1–12. https://doi.org/10.3389/fmicb.2020.00201
Weingarten EA, Atkinson CL, Jackson CR (2019) The gut microbiome of freshwater Unionidae mussels is determined by host species and is selectively retained from filtered seston. PLoS One 14(11):1–17
Weinstein MJ, Luedemann GM, Oden EM, Wagman GH, Rosselet JP, Marquez JA, Coniglio CT, Charney W, Herzog HL, Black J (1963) Gentamicin, a new antibiotic complex from Micromonospora. J Med Chem 6(4):463–464. https://doi.org/10.1021/jm00340a034
Zhang J, Guo C, Chen W, De Lajudie P, Zhang Z, Shang Y, Wang ET (2018) Mesorhizobium wenxiniae sp. nov., isolated from chickpea (Cicer arietinum L.) in China. Int J Syst Evol Microbiol 68(6):1930–1936. https://doi.org/10.1099/ijsem.0.002770
Acknowledgments
M.S. and J.W. were supported by a grant of the Deutsche Forschungsgemeinschaft (DFG STE 838/11-1; DFG WI 4609/2-1).
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2022 The Author(s), under exclusive license to Springer Nature Singapore Pte Ltd.
About this chapter
Cite this chapter
Risdian, C., Safaei, N., Steinert, M., Wink, J. (2022). Exploration of Insects and Mollusks for New Secondary Metabolites from Actinobacteria. In: Rai, R.V., Bai, J.A. (eds) Natural Products from Actinomycetes. Springer, Singapore. https://doi.org/10.1007/978-981-16-6132-7_2
Download citation
DOI: https://doi.org/10.1007/978-981-16-6132-7_2
Published:
Publisher Name: Springer, Singapore
Print ISBN: 978-981-16-6131-0
Online ISBN: 978-981-16-6132-7
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)