Deforestation impacts soil biodiversity and ecosystem services worldwide.

Deforestation poses a global threat to biodiversity and its capacity to deliver ecosystem services. Yet, the impacts of deforestation on soil biodiversity and its associated ecosystem services remain virtually unknown. We generated a global dataset including 696 paired-site observations to investigate how native forest conversion to other land uses affects soil properties, biodiversity, and functions associated with the delivery of multiple ecosystem services. The conversion of native forests to plantations, grasslands, and croplands resulted in higher bacterial diversity and more homogeneous fungal communities dominated by pathogens and with a lower abundance of symbionts. Such conversions also resulted in significant reductions in carbon storage, nutrient cycling, and soil functional rates related to organic matter decomposition. Responses of the microbial community to deforestation, including bacterial and fungal diversity and fungal guilds, were predominantly regulated by changes in soil pH and total phosphorus. Moreover, we found that soil fungal diversity and functioning in warmer and wetter native forests is especially vulnerable to deforestation. Our work highlights that the loss of native forests to managed ecosystems poses a major global threat to the biodiversity and functioning of soils and their capacity to deliver ecosystem services.

Allelopathy-selected microbiomes mitigate chemical inhibition of plant performance.

Allelopathy is a common and important stressor that shapes plant communities and can alter soil microbiomes, yet little is known about the direct effects of allelochemical addition on bacterial and fungal communities or the potential for allelochemical-selected microbiomes to mediate plant performance responses, especially in habitats naturally structured by allelopathy. Here, we present the first community-wide investigation of microbial mediation of allelochemical effects on plant performance by testing how allelopathy affects soil microbiome structure and how these microbial changes impact germination and productivity across 13 plant species. The soil microbiome exhibited significant changes to 'core' bacterial and fungal taxa, bacterial composition, abundance of functionally important bacterial and fungal taxa, and predicted bacterial functional genes after the addition of the dominant allelochemical native to this habitat. Furthermore, plant performance was mediated by the allelochemical-selected microbiome, with allelopathic inhibition of plant productivity moderately mitigated by the microbiome. Through our findings, we present a potential framework to understand the strength of plant-microbial interactions in the presence of environmental stressors, in which frequency of the ecological stress may be a key predictor of microbiome-mediation strength.

Microbiome-mediated response to pulse fire disturbance outweighs the effects of fire legacy on plant performance.

Fire plays a major role in structuring plant communities across the globe. Interactions with soil microbes impact plant fitness, scaling up to influence plant populations and distributions. Here we present the first factorial manipulation of both fire and soil microbiome presence to investigate their interactive effects on plant performance across a suite of plant species with varying life history traits. We conducted fully factorial experiments on 11 species from the Florida scrub ecosystem to test plant performance responses to soils with varying fire histories (36 soil sources), the presence/absence of a microbiome, and exposure to an experimental burn. Results revealed interactive 'pulse' effects between fire and the soil microbiome on plant performance. On average, post-fire soil microbiomes strongly reduced plant productivity compared to unburned or sterilized soils. Interestingly, longer-term fire 'legacy' effects had minor impacts on plant performance and were unrelated to soil microbiomes. While pulse fire effects on plant-microbiome interactions are short-term, they could have long-term consequences for plant communities by establishing differential microbiome-mediated priority effects during post-disturbance succession. The prominence of pulse fire effects on plant-microbe interactions has even greater import due to expected increases in fire disturbances resulting from anthropogenic climate change.

A phosphorus threshold for mycoheterotrophic plants in tropical forests.

The majority of terrestrial plants associate with arbuscular mycorrhizal (AM) fungi, which typically facilitate the uptake of limiting mineral nutrients by plants in exchange for plant carbon. However, hundreds of non-photosynthetic plant species-mycoheterotrophs-depend entirely on AM fungi for carbon as well as mineral nutrition. Mycoheterotrophs can provide insight into the operation and regulation of AM fungal relationships, but little is known about the factors, fungal or otherwise, that affect mycoheterotroph abundance and distribution. In a lowland tropical forest in Panama, we conducted the first systematic investigation into the influence of abiotic factors on the abundance and distribution of mycoheterotrophs, to ask whether the availability of nitrogen and phosphorus altered the occurrence of mycoheterotrophs and their AM fungal partners. Across a natural fertility gradient spanning the isthmus of Panama, and also in a long-term nutrient-addition experiment, mycoheterotrophs were entirely absent when soil exchangeable phosphate concentrations exceeded 2 mg P kg-1 Experimental phosphorus addition reduced the abundance of AM fungi, and also reduced the abundance of the specific AM fungal taxa required by the mycoheterotrophs, suggesting that the phosphorus sensitivity of mycoheterotrophs is underpinned by the phosphorus sensitivity of their AM fungal hosts. The soil phosphorus concentration of 2 mg P kg-1 also corresponds to a marked shift in tree community composition and soil phosphatase activity across the fertility gradient, suggesting that our findings have broad ecological significance.

Arbuscular mycorrhizal fungal community composition is altered by long-term litter removal but not litter addition in a lowland tropical forest.

Tropical forest productivity is sustained by the cycling of nutrients through decomposing organic matter. Arbuscular mycorrhizal (AM) fungi play a key role in the nutrition of tropical trees, yet there has been little experimental investigation into the role of AM fungi in nutrient cycling via decomposing organic material in tropical forests. We evaluated the responses of AM fungi in a long-term leaf litter addition and removal experiment in a tropical forest in Panama. We described AM fungal communities using 454-pyrosequencing, quantified the proportion of root length colonised by AM fungi using microscopy, and estimated AM fungal biomass using a lipid biomarker. AM fungal community composition was altered by litter removal but not litter addition. Root colonisation was substantially greater in the superficial organic layer compared with the mineral soil. Overall colonisation was lower in the litter removal treatment, which lacked an organic layer. There was no effect of litter manipulation on the concentration of the AM fungal lipid biomarker in the mineral soil. We hypothesise that reductions in organic matter brought about by litter removal may lead to AM fungi obtaining nutrients from recalcitrant organic or mineral sources in the soil, besides increasing fungal competition for progressively limited resources.

Biocrusts enhance soil organic carbon stability and regulate the fate of new-input carbon in semiarid desert ecosystems.

Given their global prevalence, dryland (including hyperarid, arid, semiarid, and dry subhumid regions) ecosystems are critical for supporting soil organic carbon (SOC) stocks, with even small changes in such SOC pools affecting the global carbon (C) cycling. Biocrusts play an essential role in supporting C cycling in semiarid ecosystems. However, the influence of biocrusts and their successional stages on SOC and its fraction contents, as well as their role in regulating new input C into SOC fractions remain largely unknown. In this study, we collected continuous samples of bare soil (BS) and three successional stages of biocrust soils (cyanobacterial (CC), low-cover moss (LM), and high-cover moss (HM)) at 0-5 cm depth every month for one year in a semiarid desert ecosystem. We analyzed SOC changes among the samples and their fraction contents including: labile organic C (LOC) (composed of microbial biomass C (MBC), dissolved organic C (DOC), and easily oxidized organic C (EOC)) and recalcitrant organic C (ROC) fractions, soil nutrient content including: ammonium (NH4+-N), nitrate (NO3--N), and available phosphorus (AP), and soil temperature and moisture. We also conducted a 13C pulse-labelling experiment in the field to accurately quantify the effects of biocrust successional stage on exogenous C allocation to SOC fractions. Our results showed that the three successional stages of biocrust (CC-LM-HM) increased SOC and ROC contents by an average of 5.3 ± 3.6 g kg-1 and 4.0 ± 3.0 g kg-1, respectively; and the MBC, DOC, and EOC contents increased by an average of 41.7 ± 24.8 mg kg-1, 28.7 ± 12.6 mg kg-1, and 1.2 ± 0.6 g kg-1, respectively, compared to that of BS. These increases were attributed to an increase in photosynthetic pigment content, higher nutrient levels, and more suitable microclimates (e.g., higher moisture and more moderate temperature) during biocrust succession. More importantly, SOC stability was greatly improved with biocrust succession from cyanobacteria to moss, as evidenced by the reduction in soil EOC:SOC and EOC:ROC ratios by an average of 50 ± 34 % and 99 ± 67 %, respectively, while the ROC:SOC ratio increased by 33 ± 16 % with biocrust succession compared to those of BS. The biocrust SOC, DOC, and MBC 13C contents at different stages were on average 0.096 ± 0.034 mg kg-1, 0.010 ± 0.005 mg kg-1, and 0.014 ± 0.005 mg kg-1 higher than those of BS. Similarly, the allocation of new-input C among the DOC and MBC at different biocrust stages (19 ± 10 %) was significantly higher than that of BS (9 ± 6 %). New-input C into the biocrusts was fixed by microbes (43 ± 18 %) within ∼10 days and converted into other forms of C (85 ± 5 %) after 80 days. Our study provides a new perspective on how biocrusts support C cycling in semiarid desert ecosystems by mediating new C inputs into diverse fractional contents, and highlights the significance of biocrust successional stages in maintaining soil C stocks and stability in the dryland soil system.

Multidimensional specialization and generalization are pervasive in soil prokaryotes.

Habitat specialization underpins biological processes from species distributions to speciation. However, organisms are often described as specialists or generalists based on a single niche axis, despite facing complex, multidimensional environments. Here, we analysed 236 environmental soil microbiomes across the United States and demonstrate that 90% of >1,200 prokaryotes followed one of two trajectories: specialization on all niche axes (multidimensional specialization) or generalization on all axes (multidimensional generalization). We then documented that this pervasive multidimensional specialization/generalization had many ecological and evolutionary consequences. First, multidimensional specialization and generalization are highly conserved with very few transitions between these two trajectories. Second, multidimensional generalists dominated communities because they were 73 times more abundant than specialists. Lastly, multidimensional specialists played important roles in community structure with ~220% more connections in microbiome networks. These results indicate that multidimensional generalization and specialization are evolutionarily stable with multidimensional generalists supporting larger populations and multidimensional specialists playing important roles within communities, probably stemming from their overrepresentation among pollutant detoxifiers and nutrient cyclers. Taken together, we demonstrate that the vast majority of soil prokaryotes are restricted to one of two multidimensional niche trajectories, multidimensional specialization or multidimensional generalization, which then has far-reaching consequences for evolutionary transitions, microbial dominance and community roles.

Acidification suppresses the natural capacity of soil microbiome to fight pathogenic Fusarium infections.

Soil-borne pathogens pose a major threat to food production worldwide, particularly under global change and with growing populations. Yet, we still know very little about how the soil microbiome regulates the abundance of soil pathogens and their impact on plant health. Here we combined field surveys with experiments to investigate the relationships of soil properties and the structure and function of the soil microbiome with contrasting plant health outcomes. We find that soil acidification largely impacts bacterial communities and reduces the capacity of soils to combat fungal pathogens. In vitro assays with microbiomes from acidified soils further highlight a declined ability to suppress Fusarium, a globally important plant pathogen. Similarly, when we inoculate healthy plants with an acidified soil microbiome, we show a greatly reduced capacity to prevent pathogen invasion. Finally, metagenome sequencing of the soil microbiome and untargeted metabolomics reveals a down regulation of genes associated with the synthesis of sulfur compounds and reduction of key traits related to sulfur metabolism in acidic soils. Our findings suggest that changes in the soil microbiome and disruption of specific microbial processes induced by soil acidification can play a critical role for plant health.

Tripartite mutualisms as models for understanding plant-microbial interactions.

All plants host diverse microbial assemblages that shape plant health, productivity, and function. While some microbial effects are attributable to particular symbionts, interactions among plant-associated microbes can nonadditively affect plant fitness and traits in ways that cannot be predicted from pairwise interactions. Recent research into tripartite plant-microbe mutualisms has provided crucial insight into this nonadditivity and the mechanisms underlying plant interactions with multiple microbes. Here, we discuss how interactions among microbial mutualists affect plant performance, highlight consequences of biotic and abiotic context-dependency for nonadditive outcomes, and summarize burgeoning efforts to determine the molecular bases of how plants regulate establishment, resource exchange, and maintenance of tripartite interactions. We conclude with four goals for future tripartite studies that will advance our overall understanding of complex plant-microbial interactions.

Plant Diversity and Fertilizer Management Shape the Belowground Microbiome of Native Grass Bioenergy Feedstocks.

Plants may actively cultivate microorganisms in their roots and rhizosphere that enhance their nutrition. To develop cropping strategies that substitute mineral fertilizers for beneficial root symbioses, we must first understand how microbial communities associated with plant roots differ among plant taxa and how they respond to fertilization. Arbuscular mycorrhizal (AM) fungi and rhizobacteria are of particular interest because they enhance nutrient availability to plants and perform a suite of nutrient cycling functions. The purpose of this experiment is to examine the root and soil microbiome in a long-term switchgrass (Panicum virgatum) biofuel feedstock experiment and determine how AM fungi and rhizobacteria respond to plant diversity and soil fertility. We hypothesize that intra- and interspecific plant diversity, nitrogen fertilization (+N), and their interaction will influence the biomass and community composition of AM fungi and rhizobacteria. We further hypothesize that +N will reduce the abundance of nitrogenase-encoding nifH genes on the rhizoplane. Roots and soils were sampled from three switchgrass cultivars (Cave-in-Rock, Kanlow, Southlow) grown in monoculture, intraspecific mixture, and interspecific planting mixtures with either Andropogon gerardii or diverse native tallgrass prairie species. Molecular sequencing was performed on root and soil samples, fatty acid extractions were assessed to determine microbial biomass, and quantitative polymerase chain reaction (qPCR) was performed on nifH genes from the rhizoplane. Sequence data determined core AM fungal and bacterial microbiomes and indicator taxa for plant diversity and +N treatments. We found that plant diversity and +N influenced AM fungal biomass and community structure. Across all plant diversity treatments, +N reduced the biomass of AM fungi and nifH gene abundance by more than 40%. The AM fungal genus Scutellospora was an indicator for +N, with relative abundance significantly greater under +N and in monoculture treatments. Community composition of rhizobacteria was influenced by plant diversity but not by +N. Verrucomicrobia and Proteobacteria were the dominant bacterial phyla in both roots and soils. Our findings provide evidence that soil fertility and plant diversity structure the root and soil microbiome. Optimization of soil communities for switchgrass production must take into account differences among cultivars and their unique responses to shifts in soil fertility.

Responses of arbuscular mycorrhizal fungi to long-term inorganic and organic nutrient addition in a lowland tropical forest.

Improved understanding of the nutritional ecology of arbuscular mycorrhizal (AM) fungi is important in understanding how tropical forests maintain high productivity on low-fertility soils. Relatively little is known about how AM fungi will respond to changes in nutrient inputs in tropical forests, which hampers our ability to assess how forest productivity will be influenced by anthropogenic change. Here we assessed the influence of long-term inorganic and organic nutrient additions and nutrient depletion on AM fungi, using two adjacent experiments in a lowland tropical forest in Panama. We characterised AM fungal communities in soil and roots using 454-pyrosequencing, and quantified AM fungal abundance using microscopy and a lipid biomarker. Phosphorus and nitrogen addition reduced the abundance of AM fungi to a similar extent, but affected community composition in different ways. Nutrient depletion (removal of leaf litter) had a pronounced effect on AM fungal community composition, affecting nearly as many OTUs as phosphorus addition. The addition of nutrients in organic form (leaf litter) had little effect on any AM fungal parameter. Soil AM fungal communities responded more strongly to changes in nutrient availability than communities in roots. This suggests that the 'dual niches' of AM fungi in soil versus roots are structured to different degrees by abiotic environmental filters, and biotic filters imposed by the plant host. Our findings indicate that AM fungal communities are fine-tuned to nutrient regimes, and support future studies aiming to link AM fungal community dynamics with ecosystem function.