The root microbiome influences scales from molecules to ecosystems: The unseen majority.

Plants are teeming with microbial organisms including those that colonize internal tissues as well as those that adhere to external surfaces. In the rhizosphere, the plant-associated microbiome is intricately involved in plant health and serves as a reservoir of additional genes that plants can access when needed. Microbiome regulation of plant trait expression affects plant performance, which in turn influences various ecosystem functions, such as primary productivity and soil health. Understanding these plant- and microbe-driven interactions requires a study of the nature and effects of the plant microbiome. Conceptualizing the microbiome requires a synthesis of microbial ecology, physiology, and bioinformatics, integrated with insight into host biology and ecology. Microbiome structure and function analyses are recognized as essential components to understand the genetic and functional capacity of the host (previously assigned solely to the host) and include vital aspects of metabolism and physiology. Here, as a special section, we present a set of papers that address the complex interactions between plants and root microbiomes in the rhizosphere. This unseen majority spans scales; with its microorganisms numerically dominant in terrestrial ecosystems, the root microbiome is also involved in plant genetics through integral roles in plant trait expression that can effect community composition and ecosystem functions, such as soil health.

Bacterial endophytes enhance competition by invasive plants.

PREMISE OF THE STUDY: Invasive plants can alter soil microbial communities and profoundly alter ecosystem processes. In the invasive grass Sorghum halepense, these disruptions are consequences of rhizome-associated bacterial endophytes. We describe the effects of N2-fixing bacterial strains from S. halepense (Rout and Chrzanowski, 2009) on plant growth and show that bacteria interact with the plant to alter soil nutrient cycles, enabling persistence of the invasive. • METHODS: We assessed fluxes in soil nutrients for ∼4 yr across a site invaded by S. halepense. We assayed the N2-fixing bacteria in vitro for phosphate solubilization, iron chelation, and production of the plant-growth hormone indole-3-acetic acid (IAA). We assessed the plant's ability to recruit bacterial partners from substrates and vertically transmit endophytes to seeds and used an antibiotic approach to inhibit bacterial activity in planta and assess microbial contributions to plant growth. • KEY RESULTS: We found persistent alterations to eight biogeochemical cycles (including nitrogen, phosphorus, and iron) in soils invaded by S. halepense. In this context, three bacterial isolates solubilized phosphate, and all produced iron siderophores and IAA in vitro. In growth chamber experiments, bacteria were transmitted vertically, and molecular analysis of bacterial community fingerprints from rhizomes indicated that endophytes are also horizontally recruited. Inhibiting bacterial activity with antibiotics resulted in significant declines in plant growth rate and biomass, with pronounced rhizome reductions. • CONCLUSIONS: This work suggests a major role of endophytes on growth and resource allocation of an invasive plant. Indeed, bacterial isolate physiology is correlated with invader effects on biogeochemical cycles of nitrogen, phosphate, and iron.

Community impacts of Prosopis juliflora invasion: biogeographic and congeneric comparisons.

We coordinated biogeographical comparisons of the impacts of an exotic invasive tree in its native and non-native ranges with a congeneric comparison in the non-native range. Prosopis juliflora is taxonomically complicated and with P. pallida forms the P. juliflora complex. Thus we sampled P. juliflora in its native Venezuela, and also located two field sites in Peru, the native range of Prosopis pallida. Canopies of Prosopis juliflora, a native of the New World but an invader in many other regions, had facilitative effects on the diversity of other species in its native Venezuela, and P. pallida had both negative and positive effects depending on the year, (overall neutral effects) in its native Peru. However, in India and Hawaii, USA, where P. juliflora is an aggressive invader, canopy effects were consistently and strongly negative on species richness. Prosopis cineraria, a native to India, had much weaker effects on species richness in India than P. juliflora. We carried out multiple congeneric comparisons between P. juliflora and P. cineraria, and found that soil from the rhizosphere of P. juliflora had higher extractable phosphorus, soluble salts and total phenolics than P. cineraria rhizosphere soils. Experimentally applied P. juliflora litter caused far greater mortality of native Indian species than litter from P. cineraria. Prosopis juliflora leaf leachate had neutral to negative effects on root growth of three common crop species of north-west India whereas P. cineraria leaf leachate had positive effects. Prosopis juliflora leaf leachate also had higher concentrations of total phenolics and L-tryptophan than P. cineraria, suggesting a potential allelopathic mechanism for the congeneric differences. Our results also suggest the possibility of regional evolutionary trajectories among competitors and that recent mixing of species from different trajectories has the potential to disrupt evolved interactions among native species.

Interactions between exotic invasive plants and soil microbes in the rhizosphere suggest that 'everything is not everywhere'.

BACKGROUND: The study of soil biota in the context of exotic plant invasions has led to an explosion in our understanding of the ecological roles of many different groups of microbes that function in roots or at the root-soil interface. Part of this progress has been the emergence of two biogeographic patterns involving invasive plants and soil microbes. First, in their non-native ranges invasive plants commonly interact differently with the same soil microbes than native plants. Second, in their native ranges, plants that are invasive elsewhere commonly interact functionally with soil microbes differently in their home ranges than they do in their non-native ranges. These studies pose a challenge to a long-held paradigm about microbial biogeography - the idea that microbes are not limited by dispersal and are thus free from the basic taxonomic, biogeographical and evolutionary framework that characterizes all other life on Earth. As an analogy, the global distribution of animals that function as carnivores does not negate the fascinating evolutionary biogeographic patterns of carnivores. Other challenges to this notion come from new measurements of genetic differences among microbes across geographic boundaries, which also suggest that meaningful biogeographic patterns exist for microorganisms. SCOPE AND CONCLUSIONS: We expand this discussion of whether or not 'everything is everywhere' by using the inherently biogeographic context of plant invasions by reviewing the literature on interactions among invasive plants and the microorganisms in the rhizosphere. We find that these interactions can be delineated at multiple scales: from individual plants to continents. Thus the microbes that regulate major aspects of plant biology do not appear to be exempt from the fundamental evolutionary processes of geographical isolation and natural selection. At the important scales of taxonomy, ecotype and ecosystem functions, the fundamental ecology of invaders and soil microbes indicates that everything might not be everywhere.