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      Application of filamentous phages in environment: A tectonic shift in the science and practice of ecorestoration

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          Abstract

          Theories in soil biology, such as plant–microbe interactions and microbial cooperation and antagonism, have guided the practice of ecological restoration (ecorestoration). Below‐ground biodiversity (bacteria, fungi, invertebrates, etc.) influences the development of above‐ground biodiversity (vegetation structure). The role of rhizosphere bacteria in plant growth has been largely investigated but the role of phages (bacterial viruses) has received a little attention. Below the ground, phages govern the ecology and evolution of microbial communities by affecting genetic diversity, host fitness, population dynamics, community composition, and nutrient cycling. However, few restoration efforts take into account the interactions between bacteria and phages. Unlike other phages, filamentous phages are highly specific, nonlethal, and influence host fitness in several ways, which make them useful as target bacterial inocula. Also, the ease with which filamentous phages can be genetically manipulated to express a desired peptide to track and control pathogens and contaminants makes them useful in biosensing. Based on ecology and biology of filamentous phages, we developed a hypothesis on the application of phages in environment to derive benefits at different levels of biological organization ranging from individual bacteria to ecosystem for ecorestoration. We examined the potential applications of filamentous phages in improving bacterial inocula to restore vegetation and to monitor changes in habitat during ecorestoration and, based on our results, recommend a reorientation of the existing framework of using microbial inocula for such restoration and monitoring. Because bacterial inocula and biomonitoring tools based on filamentous phages are likely to prove useful in developing cost‐effective methods of restoring vegetation, we propose that filamentous phages be incorporated into nature‐based restoration efforts and that the tripartite relationship between phages, bacteria, and plants be explored further. Possible impacts of filamentous phages on native microflora are discussed and future areas of research are suggested to preclude any potential risks associated with such an approach.

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          Plant-microbe interactions promoting plant growth and health: perspectives for controlled use of microorganisms in agriculture.

          Plant-associated microorganisms fulfill important functions for plant growth and health. Direct plant growth promotion by microbes is based on improved nutrient acquisition and hormonal stimulation. Diverse mechanisms are involved in the suppression of plant pathogens, which is often indirectly connected with plant growth. Whereas members of the bacterial genera Azospirillum and Rhizobium are well-studied examples for plant growth promotion, Bacillus, Pseudomonas, Serratia, Stenotrophomonas, and Streptomyces and the fungal genera Ampelomyces, Coniothyrium, and Trichoderma are model organisms to demonstrate influence on plant health. Based on these beneficial plant-microbe interactions, it is possible to develop microbial inoculants for use in agricultural biotechnology. Dependent on their mode of action and effects, these products can be used as biofertilizers, plant strengtheners, phytostimulators, and biopesticides. There is a strong growing market for microbial inoculants worldwide with an annual growth rate of approximately 10%. The use of genomic technologies leads to products with more predictable and consistent effects. The future success of the biological control industry will benefit from interdisciplinary research, e.g., on mass production, formulation, interactions, and signaling with the environment, as well as on innovative business management, product marketing, and education. Altogether, the use of microorganisms and the exploitation of beneficial plant-microbe interactions offer promising and environmentally friendly strategies for conventional and organic agriculture worldwide.
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            Plant growth-promoting rhizobacteria (PGPR): Their potential as antagonists and biocontrol agents

            Bacteria that colonize plant roots and promote plant growth are referred to as plant growth-promoting rhizobacteria (PGPR). PGPR are highly diverse and in this review we focus on rhizobacteria as biocontrol agents. Their effects can occur via local antagonism to soil-borne pathogens or by induction of systemic resistance against pathogens throughout the entire plant. Several substances produced by antagonistic rhizobacteria have been related to pathogen control and indirect promotion of growth in many plants, such as siderophores and antibiotics. Induced systemic resistance (ISR) in plants resembles pathogen-induced systemic acquired resistance (SAR) under conditions where the inducing bacteria and the challenging pathogen remain spatially separated. Both types of induced resistance render uninfected plant parts more resistant to pathogens in several plant species. Rhizobacteria induce resistance through the salicylic acid-dependent SAR pathway, or require jasmonic acid and ethylene perception from the plant for ISR. Rhizobacteria belonging to the genera Pseudomonas and Bacillus are well known for their antagonistic effects and their ability to trigger ISR. Resistance-inducing and antagonistic rhizobacteria might be useful in formulating new inoculants with combinations of different mechanisms of action, leading to a more efficient use for biocontrol strategies to improve cropping systems.
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              Pros and cons of phage therapy.

              Many publications list advantages and disadvantages associated with phage therapy, which is the use of bacterial viruses to combat populations of nuisance or pathogenic bacteria. The goal of this commentary is to discuss many of those issues in a single location. In terms of "Pros," for example, phages can be bactericidal, can increase in number over the course of treatment, tend to only minimally disrupt normal flora, are equally effective against antibiotic-sensitive and antibiotic-resistant bacteria, often are easily discovered, seem to be capable of disrupting bacterial biofilms, and can have low inherent toxicities. In addition to these assets, we consider aspects of phage therapy that can contribute to its safety, economics, or convenience, but in ways that are perhaps less essential to the phage potential to combat bacteria. For example, autonomous phage transfer between animals during veterinary application could provide convenience or economic advantages by decreasing the need for repeated phage application, but is not necessarily crucial to therapeutic success. We also consider possible disadvantages to phage use as antibacterial agents. These "Cons," however, tend to be relatively minor.
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                Author and article information

                Contributors
                radheyss26@gmail.com , rads26@hotmail.com
                mistletoe_h@hotmail.com
                Journal
                Ecol Evol
                Ecol Evol
                10.1002/(ISSN)2045-7758
                ECE3
                Ecology and Evolution
                John Wiley and Sons Inc. (Hoboken )
                2045-7758
                25 January 2019
                February 2019
                : 9
                : 4 ( doiID: 10.1002/ece3.2019.9.issue-4 )
                : 2263-2304
                Affiliations
                [ 1 ] Bioresources and Environmental Biotechnology Laboratory, Department of Environmental Studies University of Delhi Delhi India
                Author notes
                [*] [* ] Correspondence

                Radhey Shyam Sharma, Bioresources and Environmental Biotechnology Laboratory, Department of Environmental Studies, University of Delhi, Delhi, India.

                Emails: radheyss26@ 123456gmail.com ; rads26@ 123456hotmail.com

                Vandana Mishra, Bioresources and Environmental Biotechnology Laboratory, Department of Environmental Studies, University of Delhi, Delhi, India.

                Email: mistletoe_h@ 123456hotmail.com

                [†]

                Contributed equally.

                Author information
                https://orcid.org/0000-0003-1397-9230
                https://orcid.org/0000-0001-9701-1045
                https://orcid.org/0000-0002-1052-4188
                https://orcid.org/0000-0002-8173-9207
                Article
                ECE34743
                10.1002/ece3.4743
                6392359
                30847110
                743e9dff-25ee-4466-93db-06353e02e682
                © 2019 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd.

                This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

                History
                : 22 May 2017
                : 25 August 2018
                : 30 October 2018
                Page count
                Figures: 6, Tables: 7, Pages: 42, Words: 73469
                Categories
                Hypotheses
                Hypotheses
                Custom metadata
                2.0
                ece34743
                February 2019
                Converter:WILEY_ML3GV2_TO_NLMPMC version:5.6.0 mode:remove_FC converted:27.02.2019

                Evolutionary Biology
                bioremediation,biosensors,ecological theory,filamentous phages,microbial ecology and fitness,restoration ecology

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