Multi‐host lifestyle in plant‐beneficial bacteria: an evolutionary advantage for survival and dispersal?

Plants harbour a wide diversity of microorganisms that efficiently colonize different internal and external plant organs and compartments, including the phyllosphere (above‐ground plant surface), spermosphere (seeds and area surrounding seeds), endosphere (internal tissues) and rhizosphere (roots and soil in the vicinity of plant roots), establishing complex and dynamic interactions with the host plants (Trivedi et al., ²⁰²⁰). The plant microbiome plays major roles in the nutrition, growth and resistance against biotic and abiotic threats (Trivedi et al., ²⁰²⁰; Bakker and Berendsen, ²⁰²²; Yuan et al., ²⁰²²) and there is complex communication between microorganisms and their plant hosts (Berlanga‐Clavero et al., ²⁰²⁰; Rico‐Jiménez et al., ²⁰²²). Indeed, the secretion of a great variety of plant compounds directs the assembly of plant‐associated microbial communities and it has been proposed that plants produce a range of chemical signals to selectively recruit specific microorganisms in order to assemble protective microbiomes that enable them to cope with the imposed biotic and abiotic stresses (Rizaludin et al., ²⁰²¹; Rolli et al., ²⁰²¹; Trivedi et al., ²⁰²²). As a consequence of this selective pressure exerted by the plants, the microbial composition of the rhizosphere and the non‐rooted bulk soil differ – with the rhizosphere having a larger microbial abundance but lower diversity (Berlanga‐Clavero et al., ²⁰²⁰; Sokol et al., ²⁰²²).

Additionally, plants interact with higher organisms, including insects. The microbiome of a host insect is also critical for overcoming multiple stresses and plays key roles in insect metabolism, growth and defence (Engel et al., ²⁰¹⁶; Liu et al., ²⁰¹⁹). For example, specific phytotoxin‐degrading microbes present in the guts of insect herbivores confer resistance to these toxins, therefore allowing these herbivores to diversify and broaden the number of host plants (Itoh et al., ²⁰¹⁸). Notably, an increasing amount of experimental data suggests a link between the microbiota of soils, plants and plant‐associated insects (Liu et al., ²⁰¹⁹), which further reflects the complexity of interactions that occur in plant environments. In fact, a recent study revealed that monarch butterflies that feed on milkweed plants (Asclepias spp.) share a high percentage of bacterial taxa with the rhizosphere of the host plants (Hansen and Enders, 2022).

Currently, research on the transfer of microbial communities from plants to insects (and vice versa) remains almost exclusively restricted to plant pathogens and insect pests. For example, a hot topic in the recent years has been the ecology and virulence of Xylella fastidiosa – an important re‐emerging phytopathogen which is obligatorily transmitted to the host plant by xylem sap‐sucking insects (Sicard et al., ²⁰¹⁸). However, research involving interactions between insects and beneficial plant‐associated bacteria remains poorly investigated. Notably, in a recent review published in Environmental Microbiology, Pronk and co‐workers (2022) critically analyse different examples of plant‐beneficial bacteria which successfully colonize co‐occurring insects. Contrary to what occurs with their plant hosts, plant‐beneficial bacteria can establish commensal, mutualistic or pathogenic interactions with their insect hosts. One of these examples involves biocontrol rhizosphere bacteria of the Pseudomonas protegens species, which can switch from a root‐ to an insect‐associated lifestyle (and vice versa). Pseudomonas protegens isolates were shown to invade and kill insects by producing multiple bioactive molecules and exoenzymes. It was also found that P. protegens strains can multiply at high levels in the insect corpse, as a prior step to rhizosphere re‐colonization. This host alternation would potentially allow beneficial plant‐associated bacteria to successfully disperse to other plants over long distances (Pronk et al., ²⁰²²). The dual lifestyle of plant‐ and insect‐associated bacteria was also analysed and discussed by Pronk et al. (2022) for strains belonging to the Bacillus, Burkholderia, Photorhabdus and Streptomyces genera. Remarkably, the authors present experimental data suggesting that not only bacterial metabolic versatility but also bacterial traits like motility, biofilm formation, iron uptake and the biosynthesis of bioactive secondary metabolites impact bacterial adaptation to a multi‐host lifestyle (Pronk et al., ²⁰²²). Current hypotheses indicate that beneficial plant‐associated bacteria use this multi‐host evolutionary strategy to ensure survival in highly changing environmental niches (e.g. phyllosphere, rhizosphere).

Current estimates indicate that 75% of leading crops worldwide and 87% of flowering plants depend on animal pollinators for reproduction (Liu et al., ²⁰¹⁹; Parreño et al., ²⁰²²). Alarmingly, insect pollinator populations are severely declining as a result of the excessive use of agrochemicals, pathogens, the introduction of invasive species and climate change (Hertel et al., ²⁰²¹; Parreño et al., ²⁰²²) – an issue that will seriously affect global crop productivity and our capacity to feed the world's growing population. The decline of pollinating insects populations has been also associated with changes in their gut microbiomes (Raymann and Moran, 2018). In this regard, nectar and pollen are a source of microbes for insect pollinators as high number of bacteria exist in floral nectar (up to 10⁷ CFU mm⁻³) and pollen (10⁴–10⁷ CFU g⁻¹) (Liu et al., ²⁰¹⁹). In fact, a significant number of bacterial taxa have been identified as common to honeybee populations and flowers, including different fructophilic lactic bacteria (Liu et al., ²⁰¹⁹; Crovadore et al., ²⁰²¹) – a recently discovered group of heterofermentative bacteria that prefer fructose over glucose as a carbon source (Filannino et al., ²⁰¹⁹). Yet, pollen and nectar often contain bioactive plant secondary metabolites (Schmitt et al., ²⁰²¹) as well as agrochemicals that can alter the insect microbiome composition. As a means to understand the role of specific bacterial taxa on honeybee health, a recent report in Microbial Biotechnology explored the effects of different agrochemicals and plant secondary metabolites on planktonic and biofilm growth of fructophilic lactobacilli isolated from both the gut of honeybees and bee‐collected pollen (Tlais et al., ²⁰²²). The study found that the organophosphorus pesticides glyphosate and chlorpyrifos‐methyl completely inhibited planktonic growth of Apilactobacillus kunkeei strains, a fructophilic lactobacilli species that is a frequent inhabitant of honeybees, and drastically affected their abilities to form biofilms. On the other hand, neither the insecticide imidacloprid nor the plant secondary metabolites p‐coumaric acid and nicotine affected planktonic growth of A. kunkeei. Alternatively, p‐coumaric acid and nicotine had positive effects on the growth of sessile communities. Fructophilic lactobacilli form biofilms in honeybee hosts and previous studies revealed that organophosphorus pesticides have negative impacts on the honeybee microbiome (Motta and Moran, 2020). Tlais et al. (2022) found that biofilm‐forming A. kunkeei strains are more resistant to glyphosate and chlorpyrifos‐methyl, while further studies are required to determine whether these bacteria have beneficial effects on honeybees when exposed to agrochemicals.

Land plants and insects both originated ~475 million years ago (Raven and Wagner, 2021) and the interaction between flowering plants and pollinating insects represents an extraordinary example of co‐evolution. However, what nature has built over millions of years of evolution is in serious threat as a consequence of our human activities. The anthropogenic climate change is seriously affecting global diversity, including plants, insects and their associated microbiota (Parreño et al., ²⁰²²; Trivedi et al., ²⁰²²). This partly originates in the continued overuse of chemical pesticides and fertilizers in agriculture, which results in a severe decrease in the diversity of plants and soil microorganisms and the complexity of the interaction networks between plants and microbes (Molina‐Santiago and Matilla, 2020). For this reason, we need urgent solutions to alleviate the negative effects of our human activities, and a greater understanding of plant–microbe interactions will lay the groundwork for the development of novel microorganism‐based approaches aimed at promoting plant productivity and diversity. However, beneficial rhizosphere bacteria share many traits with insect symbionts. Hence, Pronk et al. (2022) emphasized that the use of specific rhizosphere bacteria as biopesticides and plant growth promoters should be re‐evaluated since they could potentially disperse to other ecological niches with undesirable effects or have negative impacts on plant‐beneficial insect populations (e.g. pollinators). Consequently, new insights into the ecology and mechanisms that drive the multi‐host lifestyle of beneficial plant‐associated bacteria will likely advance the development of sustainable biotechnological strategies to improve agricultural production.