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

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.

Keywords: bioremediation; biosensors; ecological theory; filamentous phages; microbial ecology and fitness; restoration ecology.

Figure 1

Ecosystem and other environmental challenges for ecological restoration of degraded lands, where current techniques face challenges but filamentous phage has potential to provide solutions. FP, filamentous phage

Figure 2

An unsolved problem related to exploiting bioremediation potential of Pseudomonas in phenol contaminated field environment highlighting the potential of filamentous phage to provide solutions and path of research to arrive at them (based on Goldstein, Mallory, & Alexander, 1985; Mrozik, Miga, & Piotrowska‐Seget, 2011). FP, filamentous phage.

Figure 3

Potential significance of filamentous phages to enhance the ecological and evolutionary potential of the bacterial community to ensure vegetation development at degraded lands

Figure 4

Potential of filamentous phages to assist in the tripartite relation of phage–bacteria–plant to positively influence the upstream effects on plant health, growth, and colonization for ecosystem restoration

Figure 5

Potential significance of filamentous phages to develop efficient biomonitoring system for tracking and management of targeted inoculated strain, pathogens, and contaminants

Figure 6

Outline of multi‐branched course of research proposed with a cohesive vision for future actions for environmental application of filamentous phage (i) for improving inoculants for plant growth, (ii) for engineering filamentous phage for biosensing and bioremediation, and (iii) for preventing potential risks of filamentous phage application in the environment. FP, filamentous phage