The Role of Rhizosphere Bacteriophages in Plant Health

Highlights

• Viruses influence host fitness through direct or indirect interactions. The latter occur mostly through bacteriophages that regulate host-associated bacterial communities.

• Bacteriophages play an important role in the ecology and evolution of the host-associated microbiome and are directly linked to host fitness.

• The composition and diversity of viruses associated with the soil rhizosphere are largely unexplored.

• The rhizosphere virome might alleviate plant responses to abiotic stress, thereby influencing plant resistance and resilience to climate change scenarios.

Microbiomes and their hosts influence each other; for instance, the microbiome improves host fitness, whereas the host supports microbiome nutrition. Most studies on this topic have focused on the role of bacteria and fungi, although research on viruses that infect bacteria, known as ‘bacteriophages’ (phages), has gained importance due to the potential role bacteriophages play in the resilience and functionality of the gut microbiome. Like the gut microbiome, the rhizosphere harbors a complex microbiome, but little is known about the role of phages in this ecosystem. In this opinion, we extend the knowledge gained in human gut virus metagenomics (viromics) to disentangle the potential role of phages in driving the resilience and functionality of the rhizosphere microbiome. We propose that future comparative studies across environments are necessary to unravel the underlying mechanisms through which phages drive the composition and functionality of the rhizosphere microbiome and its interaction with the plant host. Importantly, such understanding might generate strategies to improve plant resistance and resilience in the context of climate change.

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.