Opinion
Let the Core Microbiota Be Functional

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Trends

Recent advances in next-generation sequencing technology have boosted the field of plant–microorganism interactions, especially in rhizosphere ecology.

The principle of a core microbiota has been proposed to describe the microbial community that is systematically associated with a given plant genotype.

So far, this core microbiota was mostly defined on the basis of DNA sequences with taxonomic value, and not on their functional relevance.

However, biogeography studies suggest that microbial reservoirs may differ depending upon soil types, thus questioning the universal distribution of the taxonomic core microbiota under various environmental conditions.

The microbiota recruited by a given plant genotype in different environments seems to share greater functional similarity than taxonomic similarity.

The microbial community that is systematically associated with a given host plant is called the core microbiota. The definition of the core microbiota was so far based on its taxonomic composition, but we argue that it should also be based on its functions. This so-called functional core microbiota encompasses microbial vehicles carrying replicators (genes) with essential functions for holobiont (i.e., plant plus microbiota) fitness. It builds up from enhanced horizontal transfers of replicators as well as from ecological enrichment of their vehicles. The transmission pathways of this functional core microbiota vary over plant generations according to environmental constraints and its added value for holobiont fitness.

Section snippets

Plants–Microorganisms: A Joined Success Story

Land colonization by plants has been a formidable undertaking that was made possible with the help of friendly soil mutualistic microbes. Plants sustain their microbial partners by providing them with organic carbon that is accessible directly inside plants or released by the roots in the form of rhizodeposits 1, 2. This leads to the stimulation of a range of microbial functions that modulate hormone balance, interfere with plant and microbe communication, enhance plant mineral nutrient and

The Taxonomic Core Microbiota

Plants are colonized by and interact with a high diversity of microorganisms. This microbiota influences the physiology, growth, and health of the host plant to such an extent that plants may form with their associated microbiota single entities, termed holobionts, in which plants and their microbial partners contribute positively or negatively to the overall stability and fitness of the system 4, 5. Recent studies have defined a core range of species (or proxies such as operational taxonomic

The Functional Core Microbiota

It can be argued that plant–microorganism evolution favors the recruitment of microbial populations, possibly belonging to different taxa according to the soil type, but sharing the ability to ensure favorable functions for the host plant. In this case the focus is no longer on the microbial taxa recruited by the host plant, but rather on the microorganisms that ensure key functions for holobiont fitness, especially by promoting the nutrition (mineral nutrients for plants, exudates for

Rationale for a Functional Core Microbiota

The presence of these host-associated microbial replicators coding for shared functions while being distributed among different genetic backgrounds (i.e., vehicles) has been illustrated recently. Bulgarelli et al. [21] showed that the host genotype (Hordeum vulgare) had little impact on microbial taxonomical sequences, defining here the taxonomic core microbiota, but had a great impact on sequences with functional value, defined here as the replicators of the functional core microbiota.

Transmission and Stability of the Functional Core Microbiota

The fact that similar microbial functional groups are faithfully associated with individuals in various taxa (Ulva [22], bromeliads [16], humans [24]) suggests that the functional core microbiota recruited by a given host is somehow stable over time. This stability ensues from the genetic transmission of replicators but also from non-genetic environmental transmission. This hypothesis is in line with the ‘extended synthesis of evolution’ theory based on the concept of inclusive inheritance [39]

Relevance of the Functional Core Microbiota for Agroecological Systems

Promotion of biodiversity and biotic interactions represents a major tool in agroecology for developing agricultural systems that will be more sustainable and less dependent on chemical inputs [43]. In this context, acquiring better knowledge about the functional core microbiota and ways to promote it is essential for the development of agroecological systems. This is a major paradigm shift because plant domestication may in contrario have affected the ability of plants to establish beneficial

Concluding Remarks and Future Perspectives

Plants recruit functional microbiota related to each plant genotype that can be called functional core microbiota. The plant–functional core microbiota associations with reciprocal beneficial effects will benefit from a selective advantage as compared to associations with neutral or deleterious effects. The functional core microbiota may thus ensure a better fitness of the holobiont (i.e., plant plus functional core microbiota). The core microbiota functions are coded by replicators distributed

Acknowledgments

The authors are grateful to Annie Buchwalter for helping with the English text.

Glossary

Fitness
survival and reproductive success of an individual in a given environment.
Functional core microbiota
a subset of the microbiota associated with a given host irrespective of the macroenvironment (e.g., soil type) and that encompasses microbial vehicles carrying replicators with essential functions for holobiont fitness (Table 1).
Holobiont
an entity encompassing an individual host (e.g., a plant) and its associated microbial community (i.e., the microbiota). On the basis of its properties,

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