Shifts in mycorrhizal types of fungi and plants in response to fertilisation, warming and herbivory in a tundra grassland.

Climate warming is severely affecting high-latitude regions. In the Arctic tundra, it may lead to enhanced soil nutrient availability and interact with simultaneous changes in grazing pressure. It is presently unknown how these concurrently occurring global change drivers affect the root-associated fungal communities, particularly mycorrhizal fungi, and whether changes coincide with shifts in plant mycorrhizal types. We investigated changes in root-associated fungal communities and mycorrhizal types of the plant community in a 10-yr factorial experiment with warming, fertilisation and grazing exclusion in a Finnish tundra grassland. The strongest determinant of the root-associated fungal community was fertilisation, which consistently increased potential plant pathogen abundance and had contrasting effects on the different mycorrhizal fungal types, contingent on other treatments. Plant mycorrhizal types went through pronounced shifts, with warming favouring ecto- and ericoid mycorrhiza but not under fertilisation and grazing exclusion. Combination of all treatments resulted in dominance by arbuscular mycorrhizal plants. However, shifts in plant mycorrhizal types vs fungi were mostly but not always aligned in their magnitude and direction. Our results show that our ability to predict shifts in symbiotic and antagonistic fungal communities depend on simultaneous consideration of multiple global change factors that jointly alter plant and fungal communities.

Decadal soil warming decreased vascular plant above and belowground production in a subarctic grassland by inducing nitrogen limitation.

Below and aboveground vegetation dynamics are crucial in understanding how climate warming may affect terrestrial ecosystem carbon cycling. In contrast to aboveground biomass, the response of belowground biomass to long-term warming has been poorly studied. Here, we characterized the impacts of decadal geothermal warming at two levels (on average +3.3°C and +7.9°C) on below and aboveground plant biomass stocks and production in a subarctic grassland. Soil warming did not change standing root biomass and even decreased fine root production and reduced aboveground biomass and production. Decadal soil warming also did not significantly alter the root-shoot ratio. The linear stepwise regression model suggested that following 10 yr of soil warming, temperature was no longer the direct driver of these responses, but losses of soil N were. Soil N losses, due to warming-induced decreases in organic matter and water retention capacity, were identified as key driver of the decreased above and belowground production. The reduction in fine root production was accompanied by thinner roots with increased specific root area. These results indicate that after a decade of soil warming, plant productivity in the studied subarctic grassland was affected by soil warming mainly by the reduction in soil N.

Consistent predictors of microbial community composition across spatial scales in grasslands reveal low context-dependency.

Environmental circumstances shaping soil microbial communities have been studied extensively. However, due to disparate study designs, it has been difficult to resolve whether a globally consistent set of predictors exists, or context-dependency prevails. Here, we used a network of 18 grassland sites (11 of those containing regional plant productivity gradients) to examine (i) if similar abiotic or biotic factors predict both large-scale (across sites) and regional-scale (within sites) patterns in bacterial and fungal community composition, and (ii) if microbial community composition differs consistently at two levels of regional plant productivity (low vs. high). Our results revealed that bacteria were associated with particular soil properties (such as base saturation) and both bacteria and fungi were associated with plant community composition across sites and within the majority of sites. Moreover, a discernible microbial community signal emerged, clearly distinguishing high and low-productivity soils across different grasslands independent of their location in the world. Hence, regional productivity differences may be typified by characteristic soil microbial communities across the grassland biome. These results could encourage future research aiming to predict the general effects of global changes on soil microbial community composition in grasslands and to discriminate fertile from infertile systems using generally applicable microbial indicators.

Biochemical composition changes can be linked to the tolerance of four grassland species under more persistent precipitation regimes.

Climate models suggest that the persistence of summer precipitation regimes (PRs) is on the rise, characterized by both longer dry and longer wet durations. These PR changes may alter plant biochemical composition and thereby their economic and ecological characteristics. However, impacts of PR persistence have primarily been studied at the community level, largely ignoring the biochemistry of individual species. Here, we analyzed biochemical components of four grassland species with varying sensitivity to PR persistence (Holcus lanatus, Phleum pratense, Lychnis flos-cuculi, Plantago lanceolata) along a range of increasingly persistent PRs (longer consecutive dry and wet periods) in a mesocosm experiment. The more persistent PRs decreased nonstructural sugars, whereas they increased lignin in all species, possibly reducing plant quality. The most sensitive species Lychnis seemed less capable of altering its biochemical composition in response to altered PRs, which may partly explain its higher sensitivity. The more tolerant species may have a more robust and dynamic biochemical network, which buffers the effects of changes in individual biochemical components on biomass. We conclude that the biochemical composition changes are important determinants for plant performance under increasingly persistent precipitation regimes.

Is the climate change mitigation effect of enhanced silicate weathering governed by biological processes?

A number of negative emission technologies (NETs) have been proposed to actively remove CO2 from the atmosphere, with enhanced silicate weathering (ESW) as a relatively new NET with considerable climate change mitigation potential. Models calibrated to ESW rates in lab experiments estimate the global potential for inorganic carbon sequestration by ESW at about 0.5-5 Gt CO2  year-1 , suggesting ESW could be an important component of the future NETs mix. In real soils, however, weathering rates may differ strongly from lab conditions. Research on natural weathering has shown that biota such as plants, microbes, and macro-invertebrates can strongly affect weathering rates, but biotic effects were excluded from most ESW lab assessments. Moreover, ESW may alter soil organic carbon sequestration and greenhouse gas emissions by influencing physicochemical and biological processes, which holds the potential to perpetuate even larger negative emissions. Here, we argue that it is likely that the climate change mitigation effect of ESW will be governed by biological processes, emphasizing the need to put these processes on the agenda of this emerging research field.

Shifts in the Rhizosphere and Endosphere Colonizing Bacterial Communities Under Drought and Salinity Stress as Affected by a Biofertilizer Consortium.

The present research asks how plant growth-promoting bacterial (PGPB) inoculants and chemical fertilizers change rhizosphere and root endophytic bacterial communities in durum wheat, and its dependence on environmental stress. A greenhouse experiment was carried out under drought (at 40% field capacity), or salinity (150 mM NaCl) conditions to investigate the effects of a chemical fertilizer (containing nitrogen, phosphorus, potassium and zinc) or a biofertilizer (a bacterial consortium of four PGPBs). High-throughput amplicon sequencing of the 16S rRNA of the rhizosphere, non-sterilized, or surface-sterilized roots, showed shifts in bacterial communities in response to stress treatments, which were greater for salinity than for drought and tended to show increased oligotrophs relative abundances compared to non-stress controls. The results also showed that Proteobacteria, Acidobacteria, Bacteroidetes, Gemmatimonadetes, Thaumarchaeota, Firmicutes, and Verrucomicrobia had a higher relative abundance in the rhizosphere, while Actinobacteria were more abundant on roots, while Candidatus_Saccharibacteria and Planctomycetes inside roots. The results indicated that the root endophytic bacterial communities were more affected by (bio-) fertilization treatments than those in the rhizosphere, particularly as affected by PGPB inoculation. This greater susceptibility of endophytes to (bio-) fertilizers was associated with increased abundance of the 16S rRNA and acdS genes in plant roots, especially under stress conditions. These changes in root endophytes, which coincided with an improvement in grain yield and photosynthetic capacity of plants, may be considered as one of the mechanisms by which PGPB affect plants.

Biofertilisation with a consortium of growth-promoting bacterial strains improves the nutritional status of wheat grain under control, drought, and salinity stress conditions.

We investigated the effect of plant growth-promoting bacterial strains (PGPB) as biofertilisers on the grain metabolic composition of durum wheat (Triticum durum Desf.). To this aim, we conducted a greenhouse experiment where we grew durum wheat plants supplied with a biofertiliser consortium of four PGPB and/or chemical fertiliser (containing nitrogen, phosphorus, potassium, and zinc), under non-stress, drought (at 40% field capacity), or salinity (150 mM NaCl) conditions. Nutrient accumulations in the grain were increased in plants treated with the biofertiliser consortium, alone or with a half dose of chemical fertilisers, compared to those in no fertilisation treatment. A clear benefit of biofertiliser application in the improvement of protein, soluble sugar, starch, and lipid contents in the grains was observed in comparison with untreated controls, especially under stress conditions. The most striking observation was the absence of significant differences between biofertiliser and chemical fertiliser treatments for most parameters. Moreover, the overall response to the biofertiliser consortium was accompanied by greater changes in amino acids, organic acids, and fatty acid profiles. In conclusion, PGPB improved the metabolic and nutrient status of durum wheat grains to a similar extent as chemical fertilisers, particularly under stress conditions, demonstrating the value of PGPB as a sustainable fertilisation treatment.

Soil properties as key predictors of global grassland production: Have we overlooked micronutrients?

Fertilisation experiments have demonstrated that nutrient availability is a key determinant of biomass production and carbon sequestration in grasslands. However, the influence of nutrients in explaining spatial variation in grassland biomass production has rarely been assessed. Using a global dataset comprising 72 sites on six continents, we investigated which of 16 soil factors that shape nutrient availability associate most strongly with variation in grassland aboveground biomass. Climate and N deposition were also considered. Based on theory-driven structural equation modelling, we found that soil micronutrients (particularly Zn and Fe) were important predictors of biomass and, together with soil physicochemical properties and C:N, they explained more unique variation (32%) than climate and N deposition (24%). However, the association between micronutrients and biomass was absent in grasslands limited by NP. These results highlight soil properties as key predictors of global grassland biomass production and point to serial co-limitation by NP and micronutrients.

The role of arbuscular mycorrhizal fungi in nonnative plant invasion along mountain roads.

Plant associated mutualists can mediate invasion success by affecting the ecological niche of nonnative plant species. Anthropogenic disturbance is also key in facilitating invasion success through changes in biotic and abiotic conditions, but the combined effect of these two factors in natural environments is understudied. To better understand this interaction, we investigated how disturbance and its interaction with mycorrhizas could impact range dynamics of nonnative plant species in the mountains of Norway. Therefore, we studied the root colonisation and community composition of arbuscular mycorrhizal (AM) fungi in disturbed vs undisturbed plots along mountain roads. We found that roadside disturbance strongly increases fungal diversity and richness while also promoting AM fungal root colonisation in an otherwise ecto-mycorrhiza and ericoid-mycorrhiza dominated environment. Surprisingly, AM fungi associating with nonnative plant species were present across the whole elevation gradient, even above the highest elevational limit of nonnative plants, indicating that mycorrhizal fungi are not currently limiting the upward movement of nonnative plants. We conclude that roadside disturbance has a positive effect on AM fungal colonisation and richness, possibly supporting the spread of nonnative plants, but that there is no absolute limitation of belowground mutualists, even at high elevation.

Risk of short-term biodiversity loss under more persistent precipitation regimes.

Recent findings indicate that atmospheric warming increases the persistence of weather patterns in the mid-latitudes, resulting in sequences of longer dry and wet periods compared to historic averages. The alternation of progressively longer dry and wet extremes could increasingly select for species with a broad environmental tolerance. As a consequence, biodiversity may decline. Here we explore the relationship between the persistence of summer precipitation regimes and plant diversity by subjecting experimental grassland mesocosms to a gradient of dry-wet alternation frequencies whilst keeping the total precipitation constant. The gradient varied the duration of consecutive wet and dry periods, from 1 up to 60 days with or without precipitation, over a total of 120 days. An alternation of longer dry and wet spells led to a severe loss of species richness (up to -75% relative to the current rainfall pattern in W-Europe) and functional diversity (enhanced dominance of grasses relative to nitrogen (N)-fixers and non-N-fixing forbs). Loss of N-fixers and non-N-fixing forbs in severe treatments was linked to lower baseline competitive success and higher physiological sensitivity to changes in soil moisture compared to grasses. The extent of diversity losses also strongly depended on the timing of the dry and wet periods. Regimes in which long droughts (≥20 days) coincided with above-average temperatures showed significantly more physiological plant stress over the experimental period, greater plant mortality, and impoverished communities by the end of the season. Across all regimes, the duration of the longest period below permanent wilting point was an accurate predictor of mortality across the communities, indicating that increasingly persistent precipitation regimes may reduce opportunities for drought stress alleviation. We conclude that without recruitment, which was precluded in this experiment, summer precipitation regimes with longer dry and wet spells will likely diminish plant diversity, at least in the short term.

Initial soil community drives heathland fungal community trajectory over multiple years through altered plant-soil interactions.

Dispersal limitation, biotic interactions, and environmental filters interact to drive plant and fungal community assembly, but their combined effects are rarely investigated. This study examines how different heathland plant and fungal colonization scenarios realized via three biotic treatments - addition of mature heathland-derived sod, addition of hay, and no additions - affect soil fungal community development over 6 yr along a manipulated pH gradient in a large-scale experiment starting from an agricultural, topsoil removed state. Our results show that both biotic and abiotic (pH) treatments had a persistent influence on the development of fungal communities, but that sod additions diminished the effect of abiotic treatments through time. Analysis of correlation networks between soil fungi and plants suggests that the reduced effect of pH in the sod treatment, where both soil and plant propagules were added, might be due to plant-fungal interactions since the sod additions caused stronger, more specific, and more consistent connections compared with the no addition treatment. Based on these results, we suggest that the initial availability of heathland fungal and plant taxa, which reinforce each other, can significantly steer further fungal community development to an alternative configuration, overriding the otherwise prominent effect of abiotic (pH) conditions.

Phosphorus addition increased carbon partitioning to autotrophic respiration but not to biomass production in an experiment with Zea mays.

Plant carbon (C) partitioning-the relative use of photosynthates for biomass production, respiration, and other plant functions-is a key but poorly understood ecosystem process. In an experiment with Zea mays, with or without arbuscular mycorrhizal fungi (AMF), we investigated the effect of phosphorus (P) fertilization and AMF on plant C partitioning. Based on earlier studies, we expected C partitioning to biomass production (i.e., biomass production efficiency; BPE) to increase with increasing P addition due to reduced C partitioning to AMF. However, although plant growth was clearly stimulated by P addition, BPE did not increase. Instead, C partitioning to autotrophic respiration increased. These results contrasted with our expectations and with a previous experiment in the same set-up where P addition increased BPE while no effect on autotropic respiration was found. The comparison of both experiments suggests a key role for AMF in explaining these contrasts. Whereas in the previous experiment substantial C partitioning to AMF reduced BPE under low P, in the current experiment, C partitioning to AMF was too low to directly influence BPE. Our results illustrate the complex influence of nutrient availability and mycorrhizal symbiosis on plant C partitioning.

Effects of single and multiple species inocula of arbuscular mycorrhizal fungi on the salinity tolerance of a Bangladeshi rice (Oryza sativa L.) cultivar.

Soil salinization due to sea level rise and groundwater irrigation has become an important agronomic problem in many parts of the world. Symbiosis between crop species and arbuscular mycorrhizal fungi (AMF) may alleviate salt stress-induced detrimental effects on crop growth and yield, for example, through helping the host plant to selectively absorb potassium while avoiding uptake of excessive sodium. Here, we performed a greenhouse experiment to evaluate growth, grain yield, and salt tolerance of a Bangladeshi rice cultivar under three levels of salt stress (0, 75, and 120 mM) after inoculation with three different AMF species from three different genera (Funnelliformis mosseae (BEG12), Acaulospora laevis (BEG13), and Gigaspora margarita (BEG34)), singly and in combination. We found that under salt stress, AMF inoculation enhanced total chlorophyll concentration, shoot K+/Na+ ratio, and lowered shoot Na+/root Na+ ratio, accompanied by increased root biomass, spikelet fertility, and grain yield compared with the non-inoculated control plants. Specifically, we found that the combination of BEG13 and BEG34 increased rice yield by 125 and 143% as compared with the non-inoculated controls, at the 75 and 120mM salt levels, respectively. In general, the low AMF diversity treatments (one species or a combination of two AMF species) were found to be the most effective in mediating salt stress tolerance for the majority of the measured crop performance variables. Overall, our results indicate that specific AMF species can promote the salt tolerance and productivity of rice, likely by increasing photosynthetic efficiency and restricting Na+ uptake and transport from root to shoot in AMF-inoculated plants.

Arbuscular Mycorrhizal Fungi Alter the Community Structure of Ammonia Oxidizers at High Fertility via Competition for Soil NH4.

Nitrification represents a central process in the cycling of nitrogen (N) which in high-fertility habitats can occasionally be undesirable. Here, we explore how arbuscular mycorrhiza (AM) impacts nitrification when N availability is not limiting to plant growth. We wanted to test which of the mechanisms that have been proposed in the literature best describes how AM influences nitrification. We manipulated the growth settings of Plantago lanceolata so that we could control the mycorrhizal state of our plants. AM induced no changes in the potential nitrification rates or the estimates of ammonium oxidizing (AO) bacteria. However, we could observe a moderate shift in the community of ammonia-oxidizers, which matched the shift we saw when comparing hyphosphere to rhizosphere soil samples and mirrored well changes in the availability of ammonium in soil. We interpret our results as support that it is competition for N that drives the interaction between AM and AO. Our experiment sheds light on an understudied interaction which is pertinent to typical management practices in agricultural systems.

Favorable effect of mycorrhizae on biomass production efficiency exceeds their carbon cost in a fertilization experiment.

Biomass production efficiency (BPE), the ratio of biomass production to photosynthesis, varies greatly among ecosystems and typically increases with increasing nutrient availability. Reduced carbon partitioning to mycorrhizal fungi (i.e., per unit photosynthesis) is the hypothesized underlying mechanism, as mycorrhizal abundance and plant dependence on these symbionts typically decrease with increasing nutrient availability. In a mesocosm experiment with Zea mays, we investigated the effect of nitrogen (N) and phosphorus (P) addition and of mycorrhizal inoculation on BPE. Photosynthesis and respiration were measured at mesocosm scale and at leaf scale. The growth of arbuscular mycorrhizal fungi (AMF) was assessed with ingrowth bags while also making use of the difference in δ13 C between C4 plants and C3 soil. Mesocosms without AMF, that is, with pasteurized soil, were used to further explore the role of AMF. Plant growth, photosynthesis, and BPE were positively affected by P, but not by N addition. AMF biomass also was slightly higher under P addition, but carbon partitioning to AMF was significantly lower than without P addition. Interestingly, in the absence of AMF, plants that did not receive P died prematurely. Our study confirmed the hypothesis that BPE increases with increasing nutrient availability, and that carbon partitioning to AMF plays a key role in this nutrient effect. The comparison of inoculated vs. pasteurized mesocosms further suggested a lower carbon cost of nutrient uptake via AMF than via other mechanisms under nutrient rich conditions.

Evolution of microbial markets.

Biological market theory has been used successfully to explain cooperative behavior in many animal species. Microbes also engage in cooperative behaviors, both with hosts and other microbes, that can be described in economic terms. However, a market approach is not traditionally used to analyze these interactions. Here, we extend the biological market framework to ask whether this theory is of use to evolutionary biologists studying microbes. We consider six economic strategies used by microbes to optimize their success in markets. We argue that an economic market framework is a useful tool to generate specific and interesting predictions about microbial interactions, including the evolution of partner discrimination, hoarding strategies, specialized versus diversified mutualistic services, and the role of spatial structures, such as flocks and consortia. There is untapped potential for studying the evolutionary dynamics of microbial systems. Market theory can help structure this potential by characterizing strategic investment of microbes across a diversity of conditions.

Land use influences arbuscular mycorrhizal fungal communities in the farming-pastoral ecotone of northern China.

We performed a landscape-scale investigation to compare the arbuscular mycorrhizal fungal (AMF) communities between grasslands and farmlands in the farming-pastoral ecotone of northern China. AMF richness and community composition were examined with 454 pyrosequencing. Structural equation modelling (SEM) and multivariate analyses were applied to disentangle the direct and indirect effects (mediated by multiple environmental factors) of land use on AMF. Land use conversion from grassland to farmland significantly reduced AMF richness and extraradical hyphal length density, and these land use types also differed significantly in AMF community composition. SEM showed that the effects of land use on AMF richness and hyphal length density in soil were primarily mediated by available phosphorus and soil structural quality. Soil texture was the strongest predictor of AMF community composition. Soil carbon, nitrogen and soil pH were also significantly correlated with AMF community composition, indicating that these abiotic variables could be responsible for some of the community composition differences among sites. Our study shows that land use has a partly predictable effect on AMF communities across this ecologically relevant area of China, and indicates that high soil phosphorus concentrations and poor soil structure are particularly detrimental to AMF in this fragile ecosystem.

Can permanent grassland soils with elevated organic carbon buffer negative effects of more persistent precipitation regimes on forage grass performance?

Agricultural practices enhancing soil organic carbon (SOC) show potential to buffer negative effects of climate change on forage grass performance. We tested this by subjecting five forage grass varieties differing in fodder quality and drought/flooding resistance to increased persistence in summer precipitation regimes (PR) across sandy and sandy-loam soils from either permanent (high SOC) or temporary grasslands (low SOC) in adjacent parcels. Over the course of two consecutive summers, monoculture mesocosms were subjected to rainy/dry weather alternation either every 3 days or every 30 days, whilst keeping total precipitation equal. Increased PR persistence induced species-specific drought damage and productivity declines. Soils from permanent grasslands with elevated SOC buffered plant quality, but buffering effects of SOC on drought damage, nutrient availability and yield differed between texture classes. In the more persistent PR, Festuca arundinacea FERMINA was the most productive species but had the lowest quality under both ample water supply and mild soil drought, whilst under the most intense soil droughts, Festulolium FESTILO maintained the highest yields. The hybrid Lolium × boucheanum kunth MELCOMBI had intermediate productivity and both Lolium perenne varieties showed the lowest yields under soil drought, but the highest forage quality (especially the tetraploid variety MELFORCE). Performance varied with plant maturity stage and across seasons/years and was driven by altered water and nutrient availability and related nitrogen nutrition among species during drought and upon rewetting. Moreover, whilst permanent grassland soils showed the most consistent positive effects on plant performance, their available water capacity also declined under increased PR persistence. We conclude that permanent grassland soils with historically elevated SOC likely buffer negative effects of increasing summer weather persistence on forage grass performance, but may also be more sensitive to degradation under climate change.

Soil warming increases the number of growing bacterial taxa but not their growth rates.

Soil microorganisms control the fate of soil organic carbon. Warming may accelerate their activities putting large carbon stocks at risk of decomposition. Existing knowledge about microbial responses to warming is based on community-level measurements, leaving the underlying mechanisms unexplored and hindering predictions. In a long-term soil warming experiment in a Subarctic grassland, we investigated how active populations of bacteria and archaea responded to elevated soil temperatures (+6°C) and the influence of plant roots, by measuring taxon-specific growth rates using quantitative stable isotope probing and 18O water vapor equilibration. Contrary to prior assumptions, increased community growth was associated with a greater number of active bacterial taxa rather than generally faster-growing populations. We also found that root presence enhanced bacterial growth at ambient temperatures but not at elevated temperatures, indicating a shift in plant-microbe interactions. Our results, thus, reveal a mechanism of how soil bacteria respond to warming that cannot be inferred from community-level measurements.

Unraveling microbial processes involved in carbon and nitrogen cycling and greenhouse gas emissions in rewetted peatlands by molecular biology.

Restoration of drained peatlands through rewetting has recently emerged as a prevailing strategy to mitigate excessive greenhouse gas emissions and re-establish the vital carbon sequestration capacity of peatlands. Rewetting can help to restore vegetation communities and biodiversity, while still allowing for extensive agricultural management such as paludiculture. Belowground processes governing carbon fluxes and greenhouse gas dynamics are mediated by a complex network of microbial communities and processes. Our understanding of this complexity and its multi-factorial controls in rewetted peatlands is limited. Here, we summarize the research regarding the role of soil microbial communities and functions in driving carbon and nutrient cycling in rewetted peatlands including the use of molecular biology techniques in understanding biogeochemical processes linked to greenhouse gas fluxes. We emphasize that rapidly advancing molecular biology approaches, such as high-throughput sequencing, are powerful tools helping to elucidate the dynamics of key biogeochemical processes when combined with isotope tracing and greenhouse gas measuring techniques. Insights gained from the gathered studies can help inform efficient monitoring practices for rewetted peatlands and the development of climate-smart restoration and management strategies. Supplementary Information: The online version contains supplementary material available at 10.1007/s10533-024-01122-6.