Trends in Microbiology
OpinionThe Role of Rhizosphere Bacteriophages in Plant Health
Introduction
As a nonmotile organism, plants rely on their roots for growth. Nearly half of total photosynthetically assimilated carbon is transported belowground, supporting the build-up of root biomass and the metabolic costs of a functional and balanced root system [1]. As a consequence, the soil layer surrounding the root system, also known as the rhizosphere (see Glossary), receives a huge input in C-rich molecules through rhizodeposition and contrasts greatly with the soil situated as close as 2–5 mm from the roots [2]. This elevated energetic investment orchestrated by plants modulates the composition and activity of residing microbes and represents a hot spot of microbial activity and diversity, generating what is known as the ‘rhizosphere effect’ or ‘rhizosphere priming’ [3]. Importantly, imbalanced rhizosphere microbiomes lead to a decrease in plant growth and fitness [4].
Microbiomes housed in the rhizosphere have recently been subjected to broad comparative studies, revealing general patterns in the structure, composition, dynamics, and functioning across different host species, in addition to the role of the microbiome in plant nutrition and growth (Box 1). Despite the overwhelming number of publications on microbiome–host interactions, viruses – the most abundant entity on the planet – have been left out of the equation. Viruses infect three domains of life: Bacteria, Archaea, and Eukarya. Whereas plant and animal viruses directly influence their hosts, bacteriophages or phages influence the host indirectly by interacting with the bacterial component of the microbiome.
Phages are ubiquitous, being found across ecosystems, such as marine, terrestrial, and human gut [5., 6., 7.], but due to methodological limitations, most currently available knowledge on virus metagenomes (viromes) comes from the marine environment. More recently, the relevance of viromes has reached studies focusing on the human gut, which is expected to contain about 81 000 viruses and has low virus-to-microbe ratio, indicating that lysogenic phages are favorable in high-density systems such as the human gut [8] (Box 2). Although the number of identified viruses in soils is much lower (27 000), the fact that soils harbor the highest microbial diversity (up to 1010 bacterial species/g soil) indicates that the viral abundance and diversity in soils remains largely untapped [8., 9., 10.].
In this opinion paper, we argue that phages play a critical role in influencing the dynamics of the rhizosphere microbiome. Given the lack of information on the soil virome, we borrow results obtained in the human virome to build our case. The similarities between the rhizosphere and gut systems have been elegantly addressed recently [11., 12., 13., 14.] and highlight the suitability in transposing the concepts related to the microbiome structure and function between plants and animals (Figure 1 and Box 3). We start by discussing the current knowledge on bacteriophages in the gut and rhizosphere microbiomes, their relative contribution to bacterial resilience in the context of gut dysbiosis, and how this knowledge can be transposed to plant–microbiome interactions. We summarize by proposing experimental approaches that can generate insights on the role of phages in the stabilization of the rhizosphere soil bacterial communities.
Section snippets
Bacteriophages in the Rhizosphere and the Human Gut: Abundance and Diversity
Gut bacteriophages significantly shape the structure and function of the gut microbiome, thereby contributing to human health [15,16]. It is estimated that the gut virome consists of more than 1012 virus-like particles (VLPs) residing in the human colon and 109 per gram in fecal samples [17]. Moreover, in vitro study has demonstrated phage transcytosis across epithelial cell layers from different tissues and has revealed active phages within membrane-bound vesicles, evidencing its access to the
The Role of Phages in Bacterial Community Ecology
Regardless of the ecosystem, the ecoevolutionary roles of phages are linked to the biotic and abiotic interactions associated with their lytic and lysogenic lifestyles [35,36] (Box 2). Taking the well-documented marine ecosystems as an example, phage-induced lysis controls bacterial populations, being responsible for half of the daily mortality of marine bacteria [37,38]. Moreover, viral lysis/viral shunt breakdown releases readily available labile nutrients to retrofeed the bacterial community
The Gut Virome and Human Health
From a human health perspective, several studies have revealed the importance of taking into account the dynamics of the gut virome [16]. It has been shown that healthy individuals from different countries share about 23 bacteriophages, a putative core virome of healthy gut phages, which is significantly lower in patients with Crohn disease and ulcerative colitis [15]. Indeed, the role of the virome in bacterial dysbiosis associated with gut diseases [e.g., intestinal inflammation/inflammatory
The Virome and Plant Health
Given the functional and structural similarities between the gut and rhizosphere microbiomes, one would expect an equivalent response of the phage community to the rhizosphere microbiome and plant health [53]. Rhizosphere phages can potentially modulate soil bacterial community structure and organic matter cycling; hence; they are closely involved in soil and rhizosphere functioning. Specifically, diverse and active viral populations were reported in deep terrestrial ecosystems, where they
Concluding Remarks
The soil microbiome plays an important role in regulating biogeochemical cycles and global climate as well as in sustaining plant growth. However, our current knowledge of the soil microbiome is strongly biased against the soil virome [9]. Here, we borrowed data from different environments, such as marine ecosystems and the human gut microbiome, to establish the possible effects of the virome on the ecological dynamics of the rhizosphere microbiome and host health. Future experimental
Glossary
- Auxiliary metabolic genes (AMGs)
- phage genes that affect host metabolism. They are not essential for phage replication and reproduction.
- Bacteriophages or phages
- bacteriophages are viral particles that infect bacterial cells, which are used as machinery to replicate viral particles.
- Core microbiome
- convergent set of microbial species that have been named as a concept useful to define the prevailing microbial genotypes in a given microbiome and unusually adapted to define which species must be found
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These authors are co-first authors