A Small Number of Low-abundance Bacteria Dominate Plant Species-specific Responses during Rhizosphere Colonization

Abstract

Plant growth can be affected by soil bacteria. In turn, plants are known to influence soil bacteria through rhizodeposits and changes in abiotic conditions. We aimed to quantify the phylotype richness and relative abundance of rhizosphere bacteria that are actually influenced in a plant species-specific manner and to determine the role of the disproportionately large diversity of low-abundance bacteria belonging to the rare biosphere (<0.1 relative abundance) in this process. In addition, we aimed to determine whether plant phylogeny has an influence on the plant species-specific rhizosphere bacterial community. For this purpose, 19 herbaceous plant species from five different plant orders were grown in a common soil substrate. Bacterial communities in the initial soil substrate and the established rhizosphere soils were compared by 16S rRNA gene amplicon sequencing. Only a small number of bacterial operational taxonomic units (OTUs, 97% sequence identity) responded either positively (ca. 1%) or negatively (ca. 1%) to a specific plant species. On average, 91% of plant-specific positive response OTUs comprised bacteria belonging to the rare biosphere, highlighting that low-abundance populations are metabolically active in the rhizosphere. In addition, low-abundance OTUs were in terms of their summed relative abundance major drivers of the bacterial phyla composition across the rhizosphere of all tested plant species. However, no effect of plant phylogeny could be observed on the established rhizosphere bacterial communities, neither when considering differences in the overall established rhizosphere communities nor when considering plant species-specific responders only. Our study provides a quantitative assessment of the effect of plants on their rhizosphere bacteria across multiple plant orders. Plant species-specific effects on soil bacterial communities involved only 18–111 bacterial OTUs out of several 1000s; this minority may potentially impact plant growth in plant–bacteria interactions.

Growth arrest in the active rare biosphere

“…Our results are important in the context of the increasing awareness that the microbial rare biosphere is not only the largest pool of biodiversity on Earth (1-4) but in sum of all its lowabundance members constitutes also a large part of the biomass in a given habitat (5,14).…”

“…For example, in the studied peatland, the sum of all low-abundance species made up approximately 12% of the total bacterial and archaeal 16S rRNA genes (5). In other soils, low-abundance Alphaproteobacteria and Bacteroidetes alone constituted in sum 10% and 9% of the total bacterial population, respectively, while all low-abundance populations summed up to 37% of all bacteria (14). Upon strong environmental change, low-abundance microorganisms often grow to numerically abundant populations and replace dominant species as observed for microbial community changes after an oil spill (72, 73) or in the response of soil microorganisms towards the presence of plants (14).…”

“…In other soils, low-abundance Alphaproteobacteria and Bacteroidetes alone constituted in sum 10% and 9% of the total bacterial population, respectively, while all low-abundance populations summed up to 37% of all bacteria (14). Upon strong environmental change, low-abundance microorganisms often grow to numerically abundant populations and replace dominant species as observed for microbial community changes after an oil spill (72, 73) or in the response of soil microorganisms towards the presence of plants (14). However, subtle environmental changes (5) or recurring seasonal shifts (7,9,74) often lead to rather small shifts in lowabundance populations without rare biosphere members becoming numerically dominant.…”

“…In soil environments, removal of lowabundance species by dilution-to-extinction had a positive effect on intruding species, suggesting that active low-abundance species pre-occupy ecological niches and thus slow down invasion (10)(11)(12). Soil microorganisms of low relative abundance were also shown to play a role in community-wide species interactions, e.g, by being involved in the production of antifungal compounds that protect plants from pathogens (13) or by constituting the core of microorganisms that respond to the presence of a particular plant species (14). Other examples include microorganisms with a specialized metabolism that sustain stable low-nucleic and amino acid identities (ANI, AAI) (38) between protein-coding genes of the Desulfosporosinus MAG and reference genomes were calculated as described previously (29)…”

Akkermansia and Microbial Degradation of Mucus in Cats and Dogs: Implications to the Growing Worldwide Epidemic of Pet Obesity

“…Unfortunately, we know little about the contribution of these low abundant groups to overall gut homeostasis [179]; in fact, some researchers suggest and promote the removal of low abundant microbes from analysis in order to detect "true" phylotypes [180]. This is not a trivial topic, at least in other environments such as soil it has been shown that the low-abundance bacteria play a fundamental biological role [181] and may, in fact, be keystone species regulating the function of different microbial environments, including host-associated microbiomes [182].…”