Microbial evolution and transitions along the parasite–mutualist continuum

Nature Reviews Microbiology, Journal Year: 2021, Volume and Issue: 19(10), P. 623 - 638

Published: April 19, 2021

Virtually all plants and animals, including humans, are home to symbiotic microorganisms. Symbiotic interactions can be neutral, harmful or have beneficial effects on the host organism. However, growing evidence suggests that microbial symbionts evolve rapidly, resulting in drastic transitions along parasite–mutualist continuum. In this Review, we integrate theoretical empirical findings discuss mechanisms underpinning these evolutionary shifts, as well ecological drivers why some host–microorganism may stuck at end of addition having biomedical consequences, understanding dynamic life microorganisms reveals how symbioses shape an organism's biology entire community, particularly a changing world. for organisms. Drew, Stevens King continuum, underlying changes, selective pressures involved common approaches studying them.

Language: Английский

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Mosquito Trilogy: Microbiota, Immunity and Pathogens, and Their Implications for the Control of Disease Transmission

Frontiers in Microbiology, Journal Year: 2021, Volume and Issue: 12

Published: April 6, 2021

In mosquitoes, the interaction between gut microbiota, immune system, and pathogens that these insects transmit to humans animals is regarded as a key component toward development of control strategies, aimed at reducing burden severe diseases, such malaria dengue fever. Indeed, different microorganisms from mosquito microbiota have been investigated for their ability affect important traits biology host insect, related with its survival, reproduction. Furthermore, some shown modulate response females, significantly shaping vector competence. Here, we will review current knowledge in this field, focusing on i) complex intestinal females defenses, both humoral level; ii) how issues contributes novel targeted strategies mosquito-borne diseases use paratransgenesis or taking advantage relationship Wolbachia hosts. We conclude by providing brief overview available microbiota-immune system interplay major insect vectors.

Language: Английский

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Overview of paratransgenesis as a strategy to control pathogen transmission by insect vectors

Parasites & Vectors, Journal Year: 2022, Volume and Issue: 15(1)

Published: March 31, 2022

Abstract This article presents an overview of paratransgenesis as a strategy to control pathogen transmission by insect vectors. It first briefly summarises some the disease-causing pathogens vectored insects and emphasises need for innovative methods counter threat resistance both vector pesticides therapeutic drugs. Subsequently, state art is described, which particularly ingenious method currently under development in many important that could provide additional powerful tool use integrated pest programmes. The requirements recent advances technique are detailed given microorganisms selected genetic modification, effector molecules be expressed environmental spread transgenic bacteria into wild populations. results experimental models developed with triatomines, mosquitoes, sandflies tsetse flies analysed. Finally, regulatory safety rules satisfied successful release genetically engineered organisms produced considered. Graphical

Language: Английский

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Symbionts and gene drive: two strategies to combat vector-borne disease

Trends in Genetics, Journal Year: 2022, Volume and Issue: 38(7), P. 708 - 723

Published: March 21, 2022

Safe and sustainable approaches for mosquito control are critical due to the global increasing burden of mosquito-transmitted diseases.Novel based on symbionts currently proposed modify or suppress populations Wolbachia-based methods have already achieved some success in field trials.Transgenic mosquitoes carrying gene drives that spread through a promising approach block disease transmission vector species.Transgenic-based potentially offer more power flexibility, but symbiont-based usually socially accepted well-developed. Mosquitoes bring health problems by transmitting parasites viruses such as malaria dengue. Unfortunately, current insecticide-based strategies only moderately effective because high cost resistance. Thus, scalable, sustainable, cost-effective needed mosquito-borne control. Symbiont-based genome engineering-based provide new tools show promise meeting these criteria, enabling modification suppression approaches. Symbiotic bacteria like Wolbachia maternally inherited manipulate host reproduction enhance their vertical transmission. Genome drive methods, which genetically altered alleles throughout wild populations, also proving be powerful laboratory. Here, we review latest developments both drive-based methods. We describe notable similarities, well distinctions obstacles, relating technologies. can found almost anywhere world, tropics subtropics, half world's population is under threat pathogens dengue virus (DENV), Zika (ZIKV), chikungunya (CHIKV), yellow fever, West Nile (WNV), malaria, filarial nematodes [1.World Health Organization Working Overcome Global Impact Neglected Tropical Diseases: First WHO Report Diseases. WHO, 2010Google Scholar,2.Tahir D. et al.Vector-borne nematode diseases pets humans Mediterranean Basin: an update.Vet. World. 2019; 12: 1630-1643Crossref PubMed Scopus (15) Google Scholar]. For example, DENV incidence has grown over 30-fold past 50 years, now reaching about 400 million cases per year [3.Bhatt S. al.The distribution dengue.Nature. 2013; 496: 504-507Crossref (5268) The recent ZIKV outbreak resulted hundreds thousands infections large-scale social economic disruption [4.World Virus Outbreak Response: Interim Report. 2016Google While falling southeast Asia, rising other parts world remain 'unacceptably high' according World [5.Guglielmi G. Malaria worldwide.Nature. (Published online December 4, 2019. https://doi.org/10.1038/d41586-019-03746-3)Crossref Re-emergence expansion many factors, including increased urbanization travel trade, climate change, land use pattern changes, unreliable piped water supply [6.World Vector Control Response 2017-2030. 2017Google Current strategies, long-lasting insecticide-treated bed nets, chemical insecticides, environmental management [7.Schreck C.E. Permethrin dimethyl phthalate tent fabric treatments against Aedes aegypti.J. Am. Mosq. Assoc. 1991; 7: 533-535PubMed Scholar], been unable address genetic behavioral resistance interventions [8.Succo T. al.Autochthonous Nîmes, South France, July September 2015.Euro Surveill. 2016; 21: 21Crossref (0) In addition, unintended effect important nontarget insects, pollinators [9.Ware G.W. Effects pesticides organisms.Residue Rev. 1980; 76: 173-201Crossref (49) new, urgently diseases. response this growing need, number novel technologies expanded years. Many involve release aim achieve (see Glossary) type mosquitoes. Population reduce eliminate populations. Such include sterile insect technique (SIT), incompatible (IIT), transgenic-based technologies, where insects mate with sizes next generation. Gene approaches, increase frequency multiple generations, could after single refractory resistant prevent pathogen symbiont into enable result entire becoming pathogen. review, summarize symbiont-infected transgenic focusing different varieties capabilities. early symbiont-mediated [10.Laven H. Eradication Culex pipiens fatigans cytoplasmic incompatibility.Nature. 1967; 216: 383-384Crossref (275) Scholar] was introduction nonmodified microorganisms competence (Box 1). most extensively studied system natural It may common intracellular endosymbiont arthropods nematodes, 60% all harboring [11.Hilgenboecker K. al.How species infected Wolbachia?--A statistical analysis data.FEMS Microbiol. Lett. 2008; 281: 215-220Crossref transmitted vertically from mother offspring maximize manipulating feminization, parthenogenesis, male killing, and/or incompatibility (CI). CI induced when Wolbachia-infected males uninfected females, results nonviable offspring. inhibit infection DENV, ZIKV, arboviruses, parasite (Figure 1, Key figure ) [12.Bian al.Wolbachia invades Anopheles stephensi induces refractoriness Plasmodium infection.Science. 340: 748-751Crossref (289) Scholar, 13.Dutra H.L. blocks circulating isolates Brazilian aegypti mosquitoes.Cell Host Microbe. 19: 771-774Abstract Full Text PDF 14.Hughes G.L. virulent human falciparum gambiae.PLoS Pathog. 2011; 7e1002043Crossref (214) Transfected native used Scholar,15.Zheng X. al.Incompatible techniques combined mosquitoes.Nature. 572: 56-61Crossref (212) Interestingly, species, aegypti, naturally free [16.Gloria-Soria A. al.Lack evidence (Diptera: Culicidae).J. Med. Entomol. 2018; 55: 1354-1356PubMed Scholar,17.Ross P.A. al.An elusive endosymbiont: does occur aegypti?.Ecol. Evol. 2020; 10: 1581-1591Crossref (27) providing open niche infection. there conjecture if major vectors truly [18.Chrostek E. Gerth M. Is gambiae Wolbachia?.mBio. 10e00784-19Crossref (24) reports indicate Anopheline possess high-density [19.Walker al.Stable moucheti demeilloni mosquitoes.Curr. Biol. 2021; 31: 2310-2320Abstract (12) This offers renewed medically relevant strains adapted environment. Several reviews covered progress exploit bacterium [20.Flores H.A. O'Neill S.L. Controlling vector-borne releasing modified mosquitoes.Nat. 16: 508-518Crossref (145) 21.Wang G.-H. al.Combating using technologies.Nat. Commun. 4388Crossref 22.Caragata E.P. translational science: controlling pathogens.Trends Parasitol. 37: 1050-1067Abstract Scholar].Box 1Using strategiesThe increasingly emerging interactions among hosts, infection, inspiring development [111.Gupta Nair Dynamics insect-microbiome interaction influence microbial symbiont.Front. 11: 1357Crossref (25) Most importantly, shows potential minimize problem cause minimal side effects application includes: (i) delivering directly disrupt physiology display antipathogen effects; (ii) express effector molecules, then engineered so decreased [112.Gao al.Mosquito microbiota implications control.Trends 36: 98-111Abstract (28) vectorial capacity [113.Cansado-Utrilla C. microbiome capacity: rich discovery translation.Microbiome. 9: 111Crossref (9) I).Figure 1Key figure. control.Show full caption(A) Natural bacteria-based (CI) Serratia Y1 Asaia induce immunity slow development. secondary metabolites ureilytica Su_YN1 Chromobacterium responsible antiplasmodial (DENV)-2. (B) fungus-based Wickerhamomyces anomalus secreting toxin protein Beauveria bassiana DENV-2 (ZIKV) activity inducing system. (C) insect-specific (Eilat virus, cell fusing agent Phasi Charoen-like Negevirus) arbovirus development, either alone combination. (D) Engineered AS1 proteins Dirofilaria immitis. (E) Metarhizium pingshaense-infected shorter life spans reproductive output than (F) virus-based Negevirus expressed anti-chikungunya (CHIKV) antibody CHIKV replication.View Large Image Figure ViewerDownload Hi-res image Download (PPT) I). (A) replication. Besides Wolbachia, research made rapid recently 1A,B). field-caught sinensis berghei modulating genes [23.Bai L. al.A gut symbiotic marcescens renders activation immune responses.Front. 1580Crossref interact [24.Cappelli al.Asaia activates eliciting anti-Plasmodium response: control.Front. Genet. 836Crossref (20) Symbionts not interfere pathogens, they directly. secretes antimalarial lipase kills at stages, effectively preventing [25.Gao via secretion lipase.Nat. 6: 806-817Crossref (6) [26.Wu P. commensal promotes permissiveness arboviruses.Cell 25: 101-112Abstract (76) Likewise, inhibits midgut growth displays entomopathogenic larvae adults. Romidepsin might metabolite [27.Saraiva R.G. al.Chromobacterium spp. mediate histone deacetylase inhibitor romidepsin.Sci. Rep. 8: 6176Crossref (23) Scholar]; aminopeptidase interferes attachment degradation Flavivirus E [28.Saraiva al.Aminopeptidase secreted sp. Panama degrading protein.PLoS Negl. Trop. Dis. 12e0006443Crossref fungi yeast killer strong developmental stages [29.Cappelli al.Killer yeasts exert anti-plasmodial activities mice.Parasite Vector. 329Crossref Toll/Jak-Stat pathways reduces [30.Dong Y. fungus activate toll JAK-STAT pathway-controlled anti-dengue aegypti.Insect Biochem. Mol. 2012; 42: 126-132Crossref (80) albopictus [31.Deng S.Q. al.Beauveria virus.J. Pest. Sci. 92: 781-789Crossref (8) Beyond fungi, (ISVs) arboviruses. Cell (CFAV) recognized ISV cells phenotype [32.Stollar V. Thomas V.L. An line (Peleg) causes fusion cells.Virology. 1975; 64: 367-377Crossref (167) Another ISV, Eilat (EILV), titers delay replication vitro. When were EILV, dissemination delayed heterologous interference mechanism [33.Nasar F. al.Eilat homologous interference.Am. J. Hyg. 2015; 93: 226Google Co-infection ISVs CFAV co-infection [34.Schultz M.J. al.Dual specific limits 518: 406-413Crossref (46) another discovered [35.Vasilakis N. al.Negevirus: taxon wide geographic distribution.J. Virol. 87: 2475-2488Crossref (121) cells, Mayaro [36.Patterson E.I. al.Negeviruses alphaviruses during coinfection.J. 95e0043321Crossref (2) All suggest arboviruses superinfection exclusion, needs further testing population. producing immunomodulatory molecules (termed paratransgenesis) 1C,D). After engineered, it reintroduced arthropod its There requirements candidate symbiont. First, should able stably horizontally maintain long enough [37.Wilke A.B. Marrelli M.T. Paratransgenesis: strategy control.Parasit. Vectors. 342Crossref (97) Second, easily culturable manipulatable, while reducing fitness [38.Lovett B. al.Transgenic rapidly malaria-endemic region Burkina Faso.Science. 364: 894-897Crossref (40) Third, target [39.Wang al.Driving bacteria.Science. 2017; 357: 1399-1402Crossref (116) several candidates shown attributes paratransgenesis (AS1), isolated ovaries, horizontally, facilitating Furthermore, Together, suggests bogorensis populate larval adult organs [40.Favia al.Bacteria genus associate stephensi, Asian malarial vector.Proc. Natl. Acad. U. 2007; 104: 9047-9051Crossref (296) Recently, successfully conditionally scorpine, significantly parasites, displaying reduced compared stain constitutively expressing [41.Shane J.L. al.Blood meal-induced inhibition microbiota.Nat. 4127Crossref (31) More recently, within heartworm immitis [42.Epis al.Chimeric stimulate development.Commun. 3: 105Crossref Notably, keep capability laboratory semi-field conditions Intriguingly, appear antagonistic one another. showed lower densities counterparts, removing enabled [43.Rosso al.Reduced diversity two areas invasion.Sci. 16091Crossref Scholar,44.Hughes al.Native impedes mosquitoes.Proc. 2014; 111: 12498-12503Crossref (137) Genetically pingshaense (Mp-hybrid) coluzzii had lifespans Mp-hybrid higher virulence inoculum load trial Faso Finally, modifying Negevirus, anti-CHIKV antibodies inhibited bacteria, fungus, even existing basis identified compelling genes, cifA cifB, involved induction rescue. models mechanism(s) still elucidated, expression bacterial germline recapitulate phenotype. Expression females rescues CI, intriguingly, appears coexpression cifB required [45.Beckmann J.F. deubiquitylating enzyme incompatibility.Nat. 2: 17007Crossref (181) Scholar,46.LePage D.P. al.Prophage WO Wolbachia-induced 543: 243-247Crossref (218) phenotypes replicated crosses between cif studies examining molecular accomplished flies 46.LePage 47.Shropshire J.D. al.One prophage Drosophila melanogaster.Proc. 115: 4987-4991Crossref (82) 48.Shropshire al.Evolution-guided mutagenesis proteins: identifying CifA's complex functional repertoire essential regions CifB.PLoS 16e1008794Crossref (11) recapitulated wPip (though here, CI) [49.Adams K.L. vector.Nat. M

Language: Английский

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Insights into plastic biodegradation: community composition and functional capabilities of the superworm (Zophobas morio) microbiome in styrofoam feeding trials

Microbial Genomics, Journal Year: 2022, Volume and Issue: 8(6)

Published: June 9, 2022

Plastics are inexpensive and widely used organic polymers, but their high durability hinders biodegradation. Polystyrene, including extruded polystyrene (also known as styrofoam), is among the most commonly produced plastics worldwide recalcitrant to microbial degradation. In this study, we assessed changes in gut microbiome of superworms (Zophobas morio) reared on bran, or under starvation conditions over a 3 weeks period. Superworms all diets were able complete life cycle pupae imago, although had minimal weight gains, resulting lower pupation rates compared bran worms. The change communities from baseline differed considerably between diet groups, with groups characterized by loss diversity presence opportunistic pathogens. Inferred functions enriched group included transposon movements, membrane restructuring adaptations oxidative stress. We detected several encoded enzymes reported styrene degradation abilities, supporting previous reports polystyrene-degrading bacteria superworm gut. By recovering metagenome-assembled genomes (MAGs) linked phylogeny identified genera Pseudomonas, Rhodococcus Corynebacterium that possess genes associated conclusion, our results provide first metagenomic insights into metabolic pathways degrade polystyrene. Our also confirm can survive feed, has considerable negative impacts host health.

Language: Английский

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Involvement of Microbiota in Insect Physiology: Focus on B Vitamins

mBio, Journal Year: 2022, Volume and Issue: 14(1)

Published: Dec. 13, 2022

Insects are highly successful in colonizing a wide spectrum of ecological niches and feeding on diversity diets. This is notably linked to their capacity get from microbiota any essential component lacking the diet such as vitamins amino acids. Over century research based dietary analysis, antimicrobial treatment, gnotobiotic rearing, culture-independent microbe detection progressively generated wealth information about role specific aspects insect fitness. Thanks recent increase sequencing capacities, whole-genome number symbionts has facilitated tracing biosynthesis pathways, validation experimental data evolutionary analyses. field considerable set hosts harboring or nonspecific members. Here, we review current knowledge involvement tick nutrition, with particular focus B vitamin provision. We specifically question if there specificity provision by compared redundant yet contribution microbes. successively highlight known microbial during three main life stages invertebrates: postembryonic development, adulthood, reproduction.

Language: Английский

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Role of gut symbionts of insect pests: A novel target for insect-pest control

Frontiers in Microbiology, Journal Year: 2023, Volume and Issue: 14

Published: March 13, 2023

Insects possess beneficial and nuisance values in the context of agricultural sector human life around them. An ensemble gut symbionts assists insects to adapt diverse extreme environments occupy every available niche on earth. Microbial symbiosis helps host by supplementing necessary diet elements, providing protection from predators parasitoids through camouflage, modulation signaling pathway attain homeostasis trigger immunity against pathogens, hijacking plant pathways circumvent defence, acquiring capability degrade chemical pesticides, degradation harmful pesticides. Therefore, a microbial strategy can lead overpopulation insect pests, which drastically reduce crop yield. Some studies have demonstrated increased mortality via destruction symbionts; use antibiotics. The review summarizes various roles played microbiota pests some that been conducted pest control targeting symbionts. Manipulation or exploitation alters growth population is consequently potential target for development better strategies. Methods such as CRISPR/Cas9, RNAi combining IIT SIT increase are further discussed. In ongoing management scenario, proving be reliable, eco-friendly novel approach integrated management.

Language: Английский

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Impact of intraspecific variation in insect microbiomes on host phenotype and evolution

The ISME Journal, Journal Year: 2023, Volume and Issue: 17(11), P. 1798 - 1807

Published: Sept. 2, 2023

Abstract Microbes can be an important source of phenotypic plasticity in insects. Insect physiology, behaviour, and ecology are influenced by individual variation the microbial communities held within insect gut, reproductive organs, bacteriome, other tissues. It is becoming increasingly clear how microbiome for fitness, expansion into novel ecological niches, environments. These investigations have garnered heightened interest recently, yet a comprehensive understanding intraspecific assembly function these insect-associated shape insects still lacking. Most research focuses on core associated with species ignores variation. We argue that among driver evolution, we provide examples showing such influence fitness health insects, invasions, their persistence new environments, responses to global environmental changes.

Language: Английский

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“Ectomosphere”: Insects and Microorganism Interactions

Microorganisms, Journal Year: 2023, Volume and Issue: 11(2), P. 440 - 440

Published: Feb. 9, 2023

This study focuses on interacting with insects and their ectosymbiont (

Language: Английский

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Insect Microbial Symbionts: Ecology, Interactions, and Biological Significance

Microorganisms, Journal Year: 2023, Volume and Issue: 11(11), P. 2665 - 2665

Published: Oct. 30, 2023

The guts of insect pests are typical habitats for microbial colonization and the presence bacterial species inside gut confers several potential advantages to insects. These bacteria located symbiotically digestive tracts insects help in food digestion, phytotoxin breakdown, pesticide detoxification. Different shapes chemical assets gastrointestinal have a significant impact on structure makeup population. number communities system differs owing varying shape composition tracts. Due their short generation times rapid evolutionary rates, can develop numerous metabolic pathways adapt diverse ecological niches. In addition, despite hindering insecticide management programs, they still biotechnological uses, including industrial, clinical, environmental uses. This review discusses prevalent associated with guts, mode symbiotic interaction, role resistance, various other biological significance, along knowledge gaps future perspectives. practical consequences microbiome its interaction host may lead encountering mechanisms behind evolution resistance

Language: Английский

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