The historical conditions under which bacterial lineages evolve determine their functional traits, and consequently their contribution to ecosystem functions (EFs). Under significant trait ...conservatism, which is common in prokaryotes, phylogeny may track the evolutionary history of species and predict their functionality. Productive communities can arise from: (i) the coexistence of functional, and therefore phylogenetically distant lineages, producing high EF rates at large phylogenetic diversity (PD); (ii) the dominance of productive lineages that outcompete other clades, generating high EF at low PD. Community composition will modulate the PD-EF relationship: The effects of anciently divergent lineages, whose deeply conserved functions determine the occupancy of major niches, may differ from that of recently divergent lineages showing adaptations to current conditions. We hypothesized that, in our model Mediterranean ecosystem, EF can be explained both by competitive superiority of ancient lineages and functional complementarity of recent lineages. To test this hypothesis, we sequenced a phylogenetic marker targeting bacteria across 28 soil plots and quantified EF related to microbial productivity, decomposition and nutrient cycling. Plots accumulating recently divergent lineages consistently showed higher EF levels that were slightly modified by the accumulation of ancient lineages. We discuss the assembly processes behind these phylogenetic-scale disparities and the final outcome in terms of ecosystem functioning.
Plant species identity is assumed to be a major driver of belowground microbial diversity and composition. However, diagnosing which plant functional traits are responsible for shaping microbial ...communities remains elusive. Primary succession on barren metalliferous mining substrates was selected as the framework to study above-belowground interactions, and plant functional traits that lead the successional trajectories of soil bacterial communities were identified. The impact of the plant functional group (i.e. trees, shrubs, dwarf shrubs, perennial grasses), a trait integrating the life span and morphological structure, on the bacterial primary succession was monitored. Bacterial diversity and composition was estimated along plant size gradients including over 90 scattered patches ranging from seedlings to mature multispecific patches. Soil bacterial diversity was affected by heavy metals levels and increased towards higher resource availability underneath mature patches, with stress-tolerant heterotrophs and phototrophs being replaced by competitive heterotrophs. The plant functional group modulated these general patterns and shrubs had the greatest impact belowground by inducing the largest increase in soil fertility. Functional traits related to leaf decomposability and root architecture further determined the composition and structure of bacterial communities. These results underline the importance of plant functional traits in the assembly of soil bacterial communities, and can help guiding restoration of degraded lands.
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•Soil bacterial succession is related to plants development in mine tailings.•Bacterial diversity and community structure are influenced by plant functional group.•Soil fertility and abiotic stress below canopies are important driving factors.•Leaf decomposability and root architecture are key traits in shaping soil bacteria.•Shrubs had a greater impact belowground than other plant life forms.
AIM: Phylogenetic clustering, the coexistence of evolutionarily related organisms, appears to be common in soil bacteria. This pattern has traditionally been attributed to the habitat‐filtering of ...bacteria that are able to survive under particular abiotic settings. According to the modern coexistence theory, however, phylogenetic clustering can also arise from biotic interactions such as the competitive exclusion of large clades with low competitive abilities. Here, we used phylogeny‐based methods to discern whether the coexistence of evolutionarily related soil bacteria results from abiotic and/or biotic filtering. LOCATION: Worldwide. METHODS: We performed a Bayesian meta‐analysis based on a literature review (n = 231) to assess whether the net relatedness index (NRI) or the nearest taxon index (NTI), two measures of the phylogenetic relatedness of taxa in local assemblages, deviate from those in randomly configured communities. We then sought the best abiotic (pH, total organic carbon and total nitrogen) and biotic predictors (relative abundance of Proteobacteria, Actinobacteria and Acidobacteria) of NRI and NTI. RESULTS: Phylogenetic clustering is pervasive in soil bacterial communities regardless of the spatial and taxonomic scales (NRI = 2.29; 95% CI 1.43, 3.29; P < 0.001). Clustering is accentuated by productivity; that is, more fertile soils hold communities with more closely related bacteria (estimate = 1.05 0.03, 2.15; P < 0.05). Proteobacterial abundance, which increases with organic carbon enrichment, leads to higher relatedness among coexisting bacteria (estimate = 0.1 0.02, 0.17; P < 0.01) through the competitive exclusion of distantly related deep‐branching clades. MAIN CONCLUSIONS: Our results, together with the dominance of proteobacterial lineages in soils worldwide, suggest that the overrepresentation of this clade underlies the widespread coexistence of phylogenetically related bacteria. These results are consistent with phylogenetic clustering arising via differences in competitive ability as predicted by the coexistence theory. This supports the idea that biotic filtering might have a role in driving the phylogenetic community assembly of soil prokaryotes.
Facilitation, an ecological interaction assembling plant communities worldwide, has been shown to modulate both species richness and ecosystem functions. Such a biodiversity–ecosystem functioning ...(BEF) relationship can be decomposed into different components not only related to species losses and gains but also to the identity of the species and the context in which they live. Using an extension of the classical BEF approach named CAFE (community assembly and the functioning of ecosystems), we quantified the contribution of these components to the BEF relationship in a Spanish semiarid plant community shaped by facilitation. We used species richness as a measure for biodiversity and plant cover as a proxy of multiple ecosystem functions including plant productivity, soil protection, soil fertility and microbial productivity. Nurse plants doubled the number of species that live beneath them relative to open ground, but caused a five‐fold increase in plant cover. The disproportionate increase of plant cover was a consequence of the identity of the species enhanced by nurse plants, which were more productive than the average. We discuss these results in terms of sampling effects (i.e. the higher probability of richer communities to harbour hyperproductive species) and complementary effects (i.e. richer communities enhancing productivity through resource partitioning, abiotic facilitation or biotic feedbacks). The enhancement of ecosystem functions that plant facilitation produces by incorporating species with high functional values to the community may reverberate among other trophic levels and propagate beyond the local scale where the ecological interaction is produced.
Bacterial genes responsible for resistance to antibiotic agents (ARG) are spread from livestock to soil through application of manure, threatening environmental and human health. We investigated the ...mechanisms of ARG dissemination and persistence to disentangle i) the influence of nutrients and microorganisms on the soil tetracycline (TET) resistome, and ii) the role of indigenous soil microbiota in preventing ARG spread. We analysed short-term (7 days) and persistent (84 days) effects of manure on the resistome of three antibiotic-free pasture soils. Four microcosm treatments were evaluated: control, mineral nutrient fertilization, and deposition of a layer of fresh manure onto soil or γ-irradiated soil. We quantified five TET-resistance genes, isolated 135 TET-resistant bacteria and sequenced both culturable TET-resistant and whole bacterial communities. Manure amendments, but not nutrient addition, increased the abundance of TET-r genes such as tet(Y). Such changes persisted with time, in contrast with the TET-resistant bacterial composition, which partially recovered after manure amendments. Manured γ-irradiated soils showed significantly lower nutrient content and higher TET-r gene abundance than non-irradiated soils, suggesting that native soil bacteria are essential for the fertilization effect of manure on soil as well as control the dissemination of potentially risky TET-r genes.
1. Warmer and drier conditions associated with ongoing climate change will increase abiotic stress for plants and mycorrhizal fungi in drylands world-wide, thereby potentially reducing vegetation ...cover and productivity and increasing the risk of land degradation and desertification. Rhizosphere-microbial interactions and feedbacks are critical processes that could either mitigate or aggravate the vulnerability of dryland vegetation to forecasted climate change. 2. We conducted a 4-year manipulative study in a semi-arid shrubland in the Iberian Peninsula to assess the effects of warming (c. 2.5°C; W), rainfall reduction (c. 30%; RR) and their combination (W+RR) on the performance of native shrubs (Heiianthemum squamatum) and their associated mycorrhizal fungi. 3. Warming (W and W+RR) decreased the net photosynthetic rates of H. squamatum shrubs by 31 % despite concurrent increases in stomatal conductance (c. 33%), leading to sharp decreases (c. 50%) in water use efficiency. Warming also advanced growth phenology, decreased leaf nitrogen and phosphorus contents per unit area, reduced shoot biomass production by 36% and decreased survival during a dry year in both W and W+RR plants. Plants under RR showed more moderate decreases (c. 10%-20%) in photosynthesis, stomatal conductance and shoot growth. 4. Warming, RR and W+RR altered ectomycorrhizal fungal (EMF) community structure and drastically reduced the relative abundance of EMF sequences obtained by high-throughput sequencing, a response associated with decreases in the leaf nitrogen, phosphorus and dry matter contents of their host plants. In contrast to EMF, the community structure and relative sequence abundances of other nonmycorrhizal fungal guilds were not significantly affected by the climate manipulation treatments. 5. Synthesis. Our findings highlight the vulnerability of both native plants and their symbiotic mycorrhizal fungi to climate warming and drying in semi-arid shrublands, and point to the importance of a deeper understanding of plant-soil feedbacks to predict dryland vegetation responses to forecasted aridification. The interdependent responses of plants and ectomycorrhizal fungi to warming and rainfall reduction may lead to a detrimental feedback loop on vegetation productivity and nutrient pool size, which could amplify the adverse impacts of forecasted climate change on ecosystem functioning in EMF-dominated drylands.
Soil bacteria typically coexist with close relatives generating widespread phylogenetic clustering. This has been ascribed to the abiotic filtering of organisms with shared ecological tolerances. ...Recent theoretical developments suggest that competition can also explain the phylogenetic similarity of coexisting organisms by excluding large low‐competitive clades. We propose that combining the environmental patterns of traits associated with abiotic stress tolerances or competitive abilities with phylogeny and abundance data, can help discern between abiotic and biotic mechanisms underlying the coexistence of phylogenetically related bacteria. We applied this framework in a model system composed of interspersed habitats of highly contrasted productivity and comparatively dominated by biotic and abiotic processes, i.e. the plant patch‐gap mosaic typical of drylands. We examined the distribution of 15 traits and 3290 bacterial taxa in 28 plots. Communities showed a marked functional response to the environment. Conserved traits related to environmental stress tolerance (e.g. desiccation, formation of resistant structures) were differentially selected in either habitat, while competition related traits (e.g. organic C consumption, formation of nutrient‐scavenging structures) prevailed under high resource availability. Phylogenetic clustering was stronger in habitats dominated by biotic filtering, suggesting that competitive exclusion of large clades might underlie the ecological similarity of co‐occurring soil bacteria.
•Land application of two different sludges was evaluated.•Sludge stabilization process altered both sludge and soil microbial communities.•Thermophilic aerobic sludge provoked less pronounced changes ...in soil microbiota.•Changes in soil community were related to changes in soil chemical environment.•Thermophilic aerobic sludge enhanced microbial activity and plant performance.
Despite the widespread use of sewage sludge as an organic amendment to improve soil stability and plant productivity, relatively little is known about how the different sludge stabilization processes affect the microbial composition and diversity of the sludge and the soil microbial populations as well as plant performance. In this study, the effects caused by addition of thermophilic aerobic (ATAD) and mesophilic anaerobic (MAD) sludge and inorganic fertilization on soil microbial community structure and diversity was assessed by pyrosequencing of 16S and 18S rRNA genes. Melon (Cucumis melo L., cv. Giotto) was used as model crop and its performance (growth and physiological state) was monitored together with changes in soil chemical parameters. Our results showed that the stabilization process of sewage sludge determined the feasibility of the final by-product as an organic amendment by altering in different manner the soil environment and modifying the soil microbial community structure and functioning. Changes in soil microbial community were related more to changes in the soil chemical environment rather than to the introduction of sludge-borne microorganisms. We also have shown that changes in a single physicochemical parameter (electrical conductivity) due to sludge application are associated with a pronounced shift in microbial community structure and activity as well as in plant performance. Along these lines, we showed that the application of ATAD sludge into soil resulted in less pronounced changes in its chemistry and microbial community structure, while enhancing soil microbial activity and plant performance. This study shows, therefore, that ATAD sludge could be applied as an excellent alternative to MAD sludge or inorganic fertilization.
The acclimatization of methanogens to two-phase olive mill wastes (TPOMW) was investigated in pilot fermenters started up with cattle excreta (37°C) and after changing their feed to excreta plus ...TPOMW (37°C or 55°C) or TPOMW alone (37°C) until a steady state was reached (28 days). Methanogenic diversity was screened using a phylogenetic microarray (AnaeroChip), and positive targets were quantified by real-time PCR. Results revealed high phylogenetic richness, with representatives of three out of the four taxonomic orders found in digesters. Methanosarcina dominated in the starting excreta (>96% of total 16S rRNA gene copies; over 45 times more abundant than any other methanogen) at high acetate (0.21 g liter⁻¹) and ammonia N concentrations (1.3 g liter⁻¹). Codigestion at 37°C induced a 6-fold increase of Methanosarcina numbers, correlated with CH₄ production (rPearson = 0.94; P = 0.02). At 55°C, the rise in temperature and H₂ partial pressure induced a burst of Methanobacterium, Methanoculleus, Methanothermobacter, and a group of uncultured archaea. The digestion of excreta alone resulted in low but constant biogas production despite certain oscillations in the methanogenic biomass. Unsuccessful digestion of TPOMW alone was attributed to high Cu levels inducing inhibition of methanogenic activity. In conclusion, the versatile Methanosarcina immediately adapted to the shift from excreta to excreta plus TPOMW and was responsible for the stimulated CH₄ production at 37°C. Higher temperatures (55°C) fostered methanogenic diversity by promoting some H₂ scavengers while yielding the highest CH₄ production. Further testing is needed to find out whether there is a link between increased methanogenic diversity and reactor productivity.
The natural regeneration of forests in mining areas is typically hampered by edaphic stress. Semiarid conditions add a climatic stress that challenges the restoration of these harsh ecosystems. This ...is the case of Tetraclinisarticulata (Vahl) Masters mixed forests in the Western Mediterranean region colonizing mining structures abandoned three decades ago. We studied the factors controlling the natural establishment of nine shrub and tree species key in these forests in eight metal mine tailings in SE Spain. In addition, we assessed the success of reintroducing 1480 individuals of the nine species 15 months after planting in one of the tailings. Specifically, we analyzed the effect of (i) species identity in terms of sapling survival, growth, nutritional status and metal bioaccumulation, and (ii) adding organic amendments into the planting holes on the same parameters. Our results indicated that natural colonization is a recent process, with seedling cohorts that vary up to two orders of magnitude among species and a practical absence of adult plants in most species excepting T. articulata. We identified seed limitation as a key factor controlling seedling density, which was significantly explained by the distance from the border of the tailing to the closest adult out of the tailing. Soil metal concentration did not have any explanatory power on the density of naturally-established seedlings, whereas soil fertility was relevant only for Rhamnus lycioides L. Overall survival of planted individuals was over 80%, survival and growth remarkably differing among species. Organic amendments had neutral or negative effects on plant survival, but significantly increased the growth of survivors despite their modest effects on leaf nutrient contents. Most species showed high metal bioaccumulation, which was exacerbated by organic amendments. We discuss how biodiversity conservation programs can benefit from the affordable and successful plantation of stress-tolerant local species, but come at the expense of potential metal transfer through trophic webs.
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