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.

First Report of Filamentous Phages Isolated from Tunisian Orchards to Control Erwinia amylovora

“…The advantage of filamentous phages in this perspective is that after infection, the phage remains present in the bacterial cell, continuously releasing progeny into the environment, as such reducing the virulence of the population [ 39 ]. Sharma et al have argued that filamentous phages could be of interest in not only converting the bacterial host’s phenotype from virulent to avirulent, but also as biotechnological tools to transfer restriction endonuclease genes or toxin-producing genes csrA and ompF genes to the host cell or display specific antigens or silver nanoparticles to combat pathogenic bacteria [ 17 ].…”

“…Filamentous phages are highly specific and non-lethal, but they influence their host’s fitness in several ways, which make them useful in controlling bacteria [ 17 ]. In this regard, Kawasaki et al [ 18 ] characterized the genome of two filamentous phages, ϕRSS1 and ϕRSM1, infecting the phytopathogen Ralstonia solanacearum .…”

VIBRANT: automated recovery, annotation and curation of microbial viruses, and evaluation of viral community function from genomic sequences

“…Viruses harbor vast potential for diverse genetic content, arrangement, and encoded functions [14][15][16][17]. Recognizing their genetic diversity, there has been substantial interest in "mining" these viral sequences for novel anti-microbial drug candidates, enzymes for biotechnological applications, and for bioremediation [18][19][20][21][22]. Recently, it has been appreciated that viruses may directly link biogeochemical cycling of nutrients by specifically driving metabolic processes [23][24][25][26][27].…”

VIBRANT: Automated recovery, annotation and curation of microbial viruses, and evaluation of virome function from genomic sequences

“…Annotations from all three databases are used to assemble 27 metrics for the neural network classifier. Briefly the metrics are as follows: [1] total proteins, [2] total KEGG annotations, [3] sum of KEGG v-scores, [4] total Pfam annotations, [5] sum of Pfam v-scores, [6] total VOG annotations, [7] sum of VOG v-scores, [8] total KEGG integration related annotations (e.g., integrase), [9] total KEGG annotations with a v-score of zero, [10] total KEGG integration related annotations (e.g., integrase), [11] total Pfam annotations with a v-score of zero, [12] total VOG redoxin (e.g., glutaredoxin) related annotations, [13] total VOG non-integrase integration related annotations, [14] total VOG integrase annotations, [15] total VOG ribonucleotide reductase related annotations, [16] total VOG nucleotide replication (e.g., DNA polymerase) related annotations, [17] total KEGG nuclease (e.g., restriction endonuclease) related annotations, [18] total KEGG toxin/anti-toxin related annotations, [19] total VOG hallmark protein (e.g., capsid) annotations, [20] total proteins annotated by KEGG, Pfam and VOG, [21] total proteins annotated by Pfam and VOG only, [22] total proteins annotated by Pfam and KEGG only, [23] total proteins annotated by KEGG and VOG only, [24] total proteins annotated by KEGG only, [25] total proteins annotated by Pfam only, [26] total proteins annotated by VOG only, and [27] total unannotated proteins. Non-annotation features such as gene density, average gene length and strand switching were not used because they were found to decrease performance of the neural network classifier despite being differentiating features between bacteria/archaea and viruses; viruses tend to have shorter genes, less intergenic space and strand switch less frequently.…”