Interactions between bacterial and phage communities in natural environments

Nature Reviews Microbiology, Год журнала: 2021, Номер 20(1), С. 49 - 62

Опубликована: Авг. 9, 2021

Язык: Английский

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The Plant Microbiome: From Ecology to Reductionism and Beyond

Annual Review of Microbiology, Год журнала: 2020, Номер 74(1), С. 81 - 100

Опубликована: Июнь 12, 2020

Methodological advances over the past two decades have propelled plant microbiome research, allowing field to comprehensively test ideas proposed a century ago and generate many new hypotheses. Studying distribution of microbial taxa genes across habitats has revealed importance various ecological evolutionary forces shaping microbiota. In particular, selection imposed by strongly shapes diversity composition microbiota leads adaptation associated with navigating immune system utilizing plant-derived resources. Reductionist approaches demonstrated that interaction between immunity is, in fact, bidirectional plants, microbiota, environment shape complex chemical dialogue collectively orchestrates plantmicrobiome. The next stage research will require integration reductionist establish general understanding assembly function both natural managed environments.

Язык: Английский

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Microbiome Engineering: Synthetic Biology of Plant-Associated Microbiomes in Sustainable Agriculture

Trends in biotechnology, Год журнала: 2020, Номер 39(3), С. 244 - 261

Опубликована: Авг. 13, 2020

Mutualistic microbes associated with plants have enormous potential for economical and sustainable agriculture.There are two approaches to plant microbiome engineering: the bottom-up approach that involves isolating, engineering, reintroducing specific microbes, top-down synthetic ecology, using horizontal gene transfer a broad range of hosts in situ then phenotyping microbiome.Recent advances genome engineering tools, meta-omic computational genome-wide functional genomics can improve our ability engineer biocontrol, biofertilization, biostimulation, as well enhanced crop productivity yield.Various devices facilitate evaluation genetically modified before field studies.Robust biosafety, biosecurity, biocontainment strategies need be developed use environment. To support an ever-increasing population, modern agriculture faces numerous challenges pose major threats global food energy security. Plant-associated their many growth-promoting (PGP) traits, helping solve these challenges. However, results been variable, probably because poor colonization. Phytomicrobiome is emerging biology may offer ways alleviate this limitation. This review highlights recent both non-model bacteria microbiomes promote beneficial plant–microbe interactions, evaluate interactions. Biosafety, address environmental concerns also discussed. The United Nations estimates world population will 9.8 billion people by 2050 (https://population.un.org/wpp/). Agricultural must increase estimated 70% meet increasing demand food, feed, fiber, bioenergy (Global Productivity Initiative: https://globalagriculturalproductivity.org/). Because arable acreage unlikely grow [1.Bruinsma J. Crop production natural resource use.in: Bruinsma World Agriculture: Towards 2015/2030: An FAO Perspective. Earthscan Publications, 2003: 127-137Google Scholar], meeting requires achieving higher yields, currently attempted artificial fertilizers pesticides whose manufacture not sustainable. Synthetic nitrogen (N) fertilizer energy-intensive [2.Wang M. Greenhouse Gases, Regulated Emissions, Energy Use Transportation (GREET) Model: Version 1.5. Center Research, Argonne National Laboratory, 1999Google Scholar]. Phosphorous (P) potassium (K) mainly produced from finite mined resources likely depleted within 100 years. Pesticides carcinogenic, developmental, risks restricted [3.Hoppin J.A. LePrevost C.E. human health.in: Coll Wajnberg E. Environmental Pest Management: Challenges Agronomists, Ecologists, Economists Policymakers. Wiley, 2017: 251-273Crossref Google Scholar,4.Upadhayay et al.Impact pesticide exposure health effects.in: Srivastava P.K. Production: Physiological Biochemical Action. 2020: 69-88Crossref More achieve ever-higher yield urgently needed. harbor provide solutions current agricultural Although diverse ecological niches [5.Compant S. al.A on microbiome: functions trends microbial application.J. Adv. 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Bot. 2020; 71: 4591-4603Crossref 11.De Leij F.A. al.Field release wheat: establishment, survival dissemination.Nat. 1488-1492Crossref (32) 12.Jäderlund L. al.Use novel nonantibiotic triple marker cassette monitor high winter wheat field.FEMS Microbiol. Ecol. 2008; 63: 156-168Crossref (13) new excluded more-resilient existing communities [13.Shade al.Fundamentals community resistance resilience.Front. 3: 417Crossref (556) composition shaped over time through complex multilateral environment [14.Haichar F. al.Plant host habitat root exudates shape soil structure.ISME 2: 1221-1230Crossref 15.Hardoim P.R. al.The hidden plants: evolutionary considerations defining functioning endophytes.Microbiol. Mol. Biol. Rev. 2015; 79: 293-320Crossref (733) 16.Reinhold-Hurek B. al.Roots shaping hotspots activity.Annu. Phytopathol. 53: 403-424Crossref 17.Peterson S.B. al.Peptidoglycan Bacillus cereus mediates commensalism rhizosphere Cytophaga-Flavobacterium group.Appl. Environ. 2006; 72: 5421-5427Crossref (29) 18.Hu al.Root exudate metabolites drive plant–soil feedbacks growth defense microbiota.Nat. Commun. 9: 2738Crossref 19.Rodriguez P.A. al.Systems interactions.Mol. Plant. 12: 804-821Abstract 20.Dangl J.L. Jones J.D. pathogens integrated defence responses infection.Nature. 2001; 411: 826-833Crossref (2693) Finding microorganisms sustainably development, nutrition, fitness, disease control, dynamic stressful environments therefore depends developing manage phytomicrobiomes Scholar,15.Hardoim Scholar,21.Lemanceau P. al.Let core microbiota functional.Trends Sci. 2017; 22: 583-595Abstract 22.Niu al.Simplified representative maize roots.Proc. Natl. Acad. U. 114: E2450-E2459Crossref (153) 23.Zgadzaj R. nodule symbiosis Lotus japonicus drives establishment distinctive rhizosphere, root, communities.Proc. 2016; 113: E7996-E8005Crossref (102) 24.Haney C.H. al.Associations confer adaptive advantage plants.Nat. Plants. 115051Crossref Meta-omic studies tools researchers understanding among phytomicrobiomes. Knowledge derived [25.Mitter al.Plant–microbe partnerships 2020.Microb. 635-640Crossref (19) such only effective under conditions extremely complex, heterogeneous, systems. limitations, based increasingly recognized way give advantages [26.Mueller U.G. Sachs Engineering animal health.Trends 23: 606-617Abstract (183) allows laboratory selection according colonize plants, specifically basis how they deliver advantages. Researchers could potentially species locations (e.g., roots, leaves) at different developmental stages various conditions. In addition, consolidated engineered microbiomes. (GMMs) strictly regulated. since first trial evaluating syringae, which was carried out University California experimental plots 1987, academia industry investigated GMMs nearly three decades without notable accidents and/or [10.Bloch Scholar,27.De indigenous populations wheat.Appl. 61: 3443-3453Crossref Scholar,28.Wozniak C.A. al.Regulation FIFRA, FFDCA TSCA.in: McHughen Wozniak Regulation Biotechnology: States Canada. Springer, 2012: 57-94Crossref (7) suggesting might safely used regulations. These successes now motivating further exploration GMM directly environment, US agencies initiated research programs develop methodologies counter, even reverse effects. Several companies investigating sustainability, related strategies, business model Synlogic, Pivot Bio, JOYN NOVOME Biotechnologies, 64-X). near future, efforts prove safe strategy sustainability agriculture. Accordingly, we here strain make more amenable applications, discuss mitigate impacts (Figure 1). Phytomicrobiomes or top-down, illustrated Figure 2. approach, particular species, strains, organs isolated [29.Rodrigues R.R. al.COREMIC: web-tool search niche CORE MICrobiome.PeerJ. 6e4395Crossref (4) Scholar,30.Toju H. al.Core agroecosystems.Nat. 4: 247-257Crossref (152) After being carry desired reassembled (SynComs) [31.Vorholt al.Establishing causality: opportunities research.Cell 142-155Abstract (93) Plants inoculated robustly recolonize hosts. (HGT) introduce into situ. One incorporate mobile genetic elements (MGEs), integrate exogenous genes random subpopulation allow holistic study traits. Another bacteriophage (phage) systems eliminate populations, roles studied. section 2). Most focus established Escherichia coli. discover functions, engineered, but challenging organism-specific nuances hinder universal tools. host-range (BHR) plasmids one [32.Jain Broad plasmids.FEMS Lett. 2013; 348: 87-96Crossref (21) For example, BHR were microbe–microbe mediated quorum-sensing circuits [33.You al.Programmed control cell–cell communication regulated killing.Nature. 2004; 428: 868-871Crossref (477) Scholar,34.Hong S.H. al.Synthetic circuit consortial biofilm formation microfluidic device.Nat. 3613Crossref (108) Scholar] elucidate function secondary metabolite biosynthetic clusters (BGCs) providing plant-benefiting [35.Hennecke Recombinant carrying Rhizobium japonicum.Nature. 1981; 291: 354-355Crossref Scholar,36.Beyeler al.Enhanced indole-3-acetic acid CHA0 affects cucumber, does protection against Pythium rot.FEMS 1999; 28: 225-233Crossref although versatile, selective pressure necessary maintain them. Microbiome conversely, genome-level stably Fortunately, greatly improved. 3 shows useful including phage integrases, integrative conjugative (ICEs), chassis-independent recombinase-assisted (CRAGE), others [37.Ke Yoshikuni Y. Multi-chassis heterologous products.Curr. Opin. 62: 88-97Crossref (2) All single-step integration large DNA constructs >50 kb length, permit stacking multiple System depend target phyla. integrase, ICE, CRAGE commonly Actinobacteria, Firmicutes, Proteobacteria, respectively. Phage integrases catalyze efficient recombination between attachment sites attP–attB) [38.Fogg P.C. al.New applications integrases.J. 2014; 426: 2703-2716Crossref (88) versatile 3A). Streptomyces πC31 system characterization BGCs compatible Actinobacteria [39.Liu al.Rapid cloning meridamycin cluster coli−Streptomyces chromosome vector, pSBAC.J. Nat. Prod. 2009; 389-395Crossref 40.Li stepwise pristinamycin II biosynthesis pristinaespiralis combinatorial metabolic engineering.Metab. Eng. 29: 12-25Crossref (42) 41.Li al.Multiplexed site-specific overproducing bioactive actinomycetes.Metab. 40: 80-92Crossref (37) 42.Myronovskyi al.Generation cluster-free albus chassis strains improved clusters.Metab. 49: 316-324Crossref (39) A Bxb1 intN2 reliable putida [43.Elmore J.R. al.Development efficiency promoter library rapid modification KT2440.Metab. 5: 1-8Crossref commensal Bacteroides [44.Mimee al.Programming bacterium, thetaiotaomicron, sense respond stimuli murine gut microbiota.Cell Syst. 1: 62-71Abstract (128) 45.García-Bayona Comstock L.E. Streamlined manipulation Parabacteroides isolates microbiota.MBio. 10e01762-19Crossref 46.Wang al.Characterization mobilizable transposon, NBU2, carries lincomycin gene.J. Bacteriol. 2000; 182: 3559-3571Crossref (61) require native site each introduced [47.Dafhnis-Calas al.Iterative vivo assembly transgenes combining activities φC31 integrase Cre recombinase.Nucleic Acids 2005; 33: e189Crossref With systems, vector backbone remains scar Mini-Tn7 another promising transposon-based tool [48.Choi K.H. Tn 7-based broad-range system.Nat. Methods. 443-448Crossref 49.Kumar al.Mini-Tn7 vectors single copy Acinetobacter baumannii.J. 2010; 82: 296-300Crossref 50.LoVullo E.D. al.Single-copy chromosomal Francisella tularensis.Microbiology. 155: 1152-1163Crossref (48) mini-Tn7 relatively small [51.Roos K. al.Multicopy transposons selected Salmonella vaccine strain.Microb. 8: 177-187Crossref ICEs group MGEs via propagate replication 3B). They encode conjugation mediate intercellular [52.Johnson C.M. Grossman A.D. Integrative (ICEs): what do work.Annu. Genet. 577-601Crossref (168) autonomous [53.Lee al.Autonomous plasmid-like transposon.Mol. 75: 268-279Crossref Some conserved prfC, tRNA genes) range, evolved seamless mechanism 5′ end prevent disruption [54.Touchon accommodation domestication elements.Curr. 22-29Crossref (26) Scholar,55.Botelho al.Antibiotic aeruginosa – mechanisms, epidemiology evolution.Drug Resist. Updat. 44100640Crossref Other less AT-rich regions), fitness disrupting physiologically important [56.Wozniak R.A. Waldor M.K. elements: mosaic enabling lateral flow.Nat. 552-563Crossref (438) Genes encoding machinery, transposases identified incorporated domesticated mating partners, coli subtilis Scholar,57.Inda M.E. al.Emerging frontiers engineering.Trends Immunol. 952-973Abstract Scholar,58.Brophy al.Engineered inducible undomesticated bacteria.Nat. 1043-1053Crossref (40) [59.Cury al.Integrative hosts: composition, distribution organization.Nucleic 45: 8943-8956Crossref (27) recipients usually limited, drops exponentially construct size increases [58.Brophy colleagues recently CRAGE, technology enables highly accurate large, biological chromosomes 3C) [60.Wang G. al.CRAGE activation 2498-2510Crossref (16) process begins landing pad (LP) containing P1 recombinase flanked mutually exclusive loxP sites. Constructs pathways assembled accessory vectors. As proof concept, 25 γ-Proteobacteria 11 genera integrating unified LP enabled BGCs. substantially increased successful BGC harnessing regulatory physiological diversity species. extended 40 α-, β-, several Actinobacteria. CRAGE's versatility makes it microbe genomes characterizing pathway Overcoming restriction/modification common problem Unique protect them foreign DNA, limiting transformation. Riley overcame limitation evade immune Clostridium thermocellum [61.Riley L.A. al.Rational development transformation ATCC 27405 complete methylome analysis evasion restriction-modification systems.J. Ind. 46: 1435-1443Crossref corresponding methyltransferases cloned mimic C. methylome. Plasmids propagated efficiently transformed thermocellum. rhizobacteria, throughput dozen once. thousands associate natively SynComs rapidly diluted resilient pre-existing [62.Mallon impact failure: unsuccessful invasions steer away invader's niche.ISME 728-741Crossref Scholar,63.Costello E.K. application theory toward microbiome.Science. 336: 1255-1262Crossref (701) knowledge microbiomes, robust plants. frontier offers alternative recode metagenome build instead modifying enable introduction deletion minimal context [64.Sheth R.U. al.Manipulating 32: 189-200Abstract (87) Bacterial members undergo abundant HGT [65.Kommineni al.Bacteriocin augments competition enterococci mammalian gastrointestinal tract.Nature. 526: 719-722Crossref (173) MGEs, redesigned studies, conjugal donor transiently transferred across phyla those [66.Klümper al.Broad invade unexpectedly fraction community.ISME 934-945Crossref Scholar,67.Musovic al.Long-term manure plasmid uptake.Environ. Rep. 6: 125-130Crossref Based ICE subtilis, Brophy coworkers created miniaturized (mini-ICEBs1) delivery wide Firmicutes collected humans soil, variable (10−1 10−7 conjugations per donor) 3D) demonstrated (XPORT) 10 synthetically defined consortium situ, there four six s

Язык: Английский

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Tailoring plant-associated microbial inoculants in agriculture: a roadmap for successful application

Journal of Experimental Botany, Год журнала: 2020, Номер 71(13), С. 3878 - 3901

Опубликована: Март 9, 2020

Abstract Plants are now recognized as metaorganisms which composed of a host plant associated with multitude microbes that provide the variety essential functions to adapt local environment. Recent research showed remarkable importance and range microbial partners for enhancing growth health plants. However, plant–microbe holobionts influenced by many different factors, generating complex interactive systems. In this review, we summarize insights from emerging field, highlighting factors contribute recruitment, selection, enrichment, dynamic interactions plant-associated microbiota. We then propose roadmap synthetic community application aim establishing sustainable agricultural systems use communities enhance productivity plants independently chemical fertilizers pesticides. Considering global warming climate change, suggest desert can serve suitable pool potentially beneficial maintain under abiotic stress conditions. Finally, framework advancing inoculants in agriculture.

Язык: Английский

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A 2-kb Mycovirus Converts a Pathogenic Fungus into a Beneficial Endophyte for Brassica Protection and Yield Enhancement

Molecular Plant, Год журнала: 2020, Номер 13(10), С. 1420 - 1433

Опубликована: Сен. 29, 2020

Mycoviruses are viruses that infect fungi, and hypovirulence-associated mycoviruses have the potential to control fungal diseases. However, it is unclear how mycovirus-mediated hypovirulent strains live survive in field, no mycovirus has been applied for field crop protection. In this study, we found a previously identified small DNA (SsHADV-1) can convert its host, Sclerotinia sclerotiorum, from typical necrotrophic pathogen beneficial endophytic fungus. SsHADV-1 downregulates expression of key pathogenicity factor genes S. sclerotiorum during infection. When growing rapeseed, SsHADV-1-infected strain DT-8 significantly regulates rapeseed involved defense, hormone signaling, circadian rhythm pathways. As result, plant growth promoted disease resistance enhanced. Field experiments showed spraying at early flowering stage reduce severity stem rot by 67.6% improve yield 14.9%. Moreover, discovered could also other on DT-8-inoculated plants be recovered dead plants. These findings suggest may ability shape origin endophytism. Our discoveries influence endophytism offer novel strategy which mycovirus-infected used health release into field.

Язык: Английский

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Organochlorine contamination enriches virus-encoded metabolism and pesticide degradation associated auxiliary genes in soil microbiomes

The ISME Journal, Год журнала: 2022, Номер 16(5), С. 1397 - 1408

Опубликована: Янв. 17, 2022

Viruses significantly influence local and global biogeochemical cycles help bacteria to survive in different environments by encoding various auxiliary metabolic genes (AMGs) associated with energy acquisition, stress tolerance degradation of xenobiotics. Here we studied whether bacterial (dsDNA) virus encoded AMGs are enriched organochlorine pesticide (OCP) contaminated soil China if viral include linked OCP biodegradation. Using metagenomics, found that OCP-contaminated soils displayed a lower bacterial, but higher diversity viruses harbored relative abundance metabolism. Furthermore, the increased along severity contamination, several biodegradation were identified bioinformatically metagenomes. Functional assays conducted experimentally demonstrate virus-encoded L-2-haloacid dehalogenase gene (L-DEX) is responsible for precursors, improving growth at sub-inhibitory concentrations. Taken together, these results metabolism biodegradation, being more abundant diverse pesticides. Moreover, our findings highlight importance accessory ecology stressful environments, providing novel avenue using bioremediation soils.

Язык: Английский

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Rhizosphere Signaling: Insights into Plant–Rhizomicrobiome Interactions for Sustainable Agronomy

Microorganisms, Год журнала: 2022, Номер 10(5), С. 899 - 899

Опубликована: Апрель 25, 2022

Rhizospheric plant–microbe interactions have dynamic importance in sustainable agriculture systems that a reduced reliance on agrochemicals. Rhizosphere signaling focuses the between plants and surrounding symbiotic microorganisms facilitate development of rhizobiome diversity, which is beneficial for plant productivity. Plant–microbe communication comprises intricate modulate local systemic defense mechanisms to mitigate environmental stresses. This review deciphers insights into how exudation secondary metabolites can shape functions diversity root microbiome. It also elaborates rhizosphere influence growth, regulate immunity against phytopathogens, prime protection biotic abiotic stresses, along with some recent well-reported examples. A holistic understanding these help tailored microbial inoculants enhanced growth targeted disease suppression.

Язык: Английский

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Tapping the rhizosphere metabolites for the prebiotic control of soil-borne bacterial wilt disease

Nature Communications, Год журнала: 2023, Номер 14(1)

Опубликована: Июль 26, 2023

Prebiotics are compounds that selectively stimulate the growth and activity of beneficial microorganisms. The use prebiotics is a well-established strategy for managing human gut health. This concept can also be extended to plants where plant rhizosphere microbiomes improve nutrient acquisition disease resistance. However, we lack effective strategies choosing metabolites elicit desired impacts on In this study, target tomato (Solanum lycopersicum) suffering from wilt (caused by Ralstonia solanacearum) as source potential prebiotic metabolites. We identify (ribose, lactic acid, xylose, mannose, maltose, gluconolactone, ribitol) exclusively used soil commensal bacteria (not positively correlated with R. but not efficiently pathogen in vitro. Metabolites application 1 µmol g

Язык: Английский

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Mesophilic and thermophilic viruses are associated with nutrient cycling during hyperthermophilic composting

The ISME Journal, Год журнала: 2023, Номер 17(6), С. 916 - 930

Опубликована: Апрель 8, 2023

Abstract While decomposition of organic matter by bacteria plays a major role in nutrient cycling terrestrial ecosystems, the significance viruses remains poorly understood. Here we combined metagenomics and metatranscriptomics with temporal sampling to study mesophilic thermophilic their on during industrial-scale hyperthermophilic composting (HTC). Our results show that virus-bacteria density dynamics activity are tightly coupled, where specific track host densities, triggering microbial community succession via top-down control HTC. Moreover, encoded expressed several auxiliary metabolic genes (AMGs) linked carbon cycling, impacting turnover alongside bacteria. Nutrient correlated positively virus–host ratio, indicative positive relationship between ecosystem functioning, viral abundances, activity. These effects were predominantly driven DNA as most detected RNA associated eukaryotes not phase composting. findings suggest could drive HTC recycling bacterial biomass through cell lysis expressing key AMGs. Viruses hence potentially be used indicators functioning optimize productivity biotechnological agricultural systems.

Язык: Английский

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Harnessing the plant microbiome for sustainable crop production

Nature Reviews Microbiology, Год журнала: 2024, Номер unknown

Опубликована: Авг. 15, 2024

Язык: Английский

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