Revealing the transfer pathways of cyanobacterial-fixed N into the boreal forest through the feather-moss microbiome.

Introduction: Biological N2 fixation in feather-mosses is one of the largest inputs of new nitrogen (N) to boreal forest ecosystems; however, revealing the fate of newly fixed N within the bryosphere (i.e. bryophytes and their associated organisms) remains uncertain. Methods: Herein, we combined 15N tracers, high resolution secondary ion mass-spectrometry (NanoSIMS) and a molecular survey of bacterial, fungal and diazotrophic communities, to determine the origin and transfer pathways of newly fixed N2 within feather-moss (Pleurozium schreberi) and its associated microbiome. Results: NanoSIMS images reveal that newly fixed N2, derived from cyanobacteria, is incorporated into moss tissues and associated bacteria, fungi and micro-algae. Discussion: These images demonstrate that previous assumptions that newly fixed N2 is sequestered into moss tissue and only released by decomposition are not correct. We provide the first empirical evidence of new pathways for N2 fixed in feather-mosses to enter the boreal forest ecosystem (i.e. through its microbiome) and discuss the implications for wider ecosystem function.

The influence of soil age on ecosystem structure and function across biomes.

The importance of soil age as an ecosystem driver across biomes remains largely unresolved. By combining a cross-biome global field survey, including data for 32 soil, plant, and microbial properties in 16 soil chronosequences, with a global meta-analysis, we show that soil age is a significant ecosystem driver, but only accounts for a relatively small proportion of the cross-biome variation in multiple ecosystem properties. Parent material, climate, vegetation and topography predict, collectively, 24 times more variation in ecosystem properties than soil age alone. Soil age is an important local-scale ecosystem driver; however, environmental context, rather than soil age, determines the rates and trajectories of ecosystem development in structure and function across biomes. Our work provides insights into the natural history of terrestrial ecosystems. We propose that, regardless of soil age, changes in the environmental context, such as those associated with global climatic and land-use changes, will have important long-term impacts on the structure and function of terrestrial ecosystems across biomes.

Multiple elements of soil biodiversity drive ecosystem functions across biomes.

The role of soil biodiversity in regulating multiple ecosystem functions is poorly understood, limiting our ability to predict how soil biodiversity loss might affect human wellbeing and ecosystem sustainability. Here, combining a global observational study with an experimental microcosm study, we provide evidence that soil biodiversity (bacteria, fungi, protists and invertebrates) is significantly and positively associated with multiple ecosystem functions. These functions include nutrient cycling, decomposition, plant production, and reduced potential for pathogenicity and belowground biological warfare. Our findings also reveal the context dependency of such relationships and the importance of the connectedness, biodiversity and nature of the globally distributed dominant phylotypes within the soil network in maintaining multiple functions. Moreover, our results suggest that the positive association between plant diversity and multifunctionality across biomes is indirectly driven by soil biodiversity. Together, our results provide insights into the importance of soil biodiversity for maintaining soil functionality locally and across biomes, as well as providing strong support for the inclusion of soil biodiversity in conservation and management programmes.

Correction to: Long-Term Recovery of Microbial Communities in the Boreal Bryosphere Following Fire Disturbance.

The original version of this article contained an error in the Molecular Analysis subsection of the Methods.

Global ecological predictors of the soil priming effect.

Identifying the global drivers of soil priming is essential to understanding C cycling in terrestrial ecosystems. We conducted a survey of soils across 86 globally-distributed locations, spanning a wide range of climates, biotic communities, and soil conditions, and evaluated the apparent soil priming effect using 13C-glucose labeling. Here we show that the magnitude of the positive apparent priming effect (increase in CO2 release through accelerated microbial biomass turnover) was negatively associated with SOC content and microbial respiration rates. Our statistical modeling suggests that apparent priming effects tend to be negative in more mesic sites associated with higher SOC contents. In contrast, a single-input of labile C causes positive apparent priming effects in more arid locations with low SOC contents. Our results provide solid evidence that SOC content plays a critical role in regulating apparent priming effects, with important implications for the improvement of C cycling models under global change scenarios.

Changes in belowground biodiversity during ecosystem development.

Belowground organisms play critical roles in maintaining multiple ecosystem processes, including plant productivity, decomposition, and nutrient cycling. Despite their importance, however, we have a limited understanding of how and why belowground biodiversity (bacteria, fungi, protists, and invertebrates) may change as soils develop over centuries to millennia (pedogenesis). Moreover, it is unclear whether belowground biodiversity changes during pedogenesis are similar to the patterns observed for aboveground plant diversity. Here we evaluated the roles of resource availability, nutrient stoichiometry, and soil abiotic factors in driving belowground biodiversity across 16 soil chronosequences (from centuries to millennia) spanning a wide range of globally distributed ecosystem types. Changes in belowground biodiversity during pedogenesis followed two main patterns. In lower-productivity ecosystems (i.e., drier and colder), increases in belowground biodiversity tracked increases in plant cover. In more productive ecosystems (i.e., wetter and warmer), increased acidification during pedogenesis was associated with declines in belowground biodiversity. Changes in the diversity of bacteria, fungi, protists, and invertebrates with pedogenesis were strongly and positively correlated worldwide, highlighting that belowground biodiversity shares similar ecological drivers as soils and ecosystems develop. In general, temporal changes in aboveground plant diversity and belowground biodiversity were not correlated, challenging the common perception that belowground biodiversity should follow similar patterns to those of plant diversity during ecosystem development. Taken together, our findings provide evidence that ecological patterns in belowground biodiversity are predictable across major globally distributed ecosystem types and suggest that shifts in plant cover and soil acidification during ecosystem development are associated with changes in belowground biodiversity over centuries to millennia.

Long-Term Recovery of Microbial Communities in the Boreal Bryosphere Following Fire Disturbance.

Our study used a ∼360-year fire chronosequence in northern Sweden to investigate post-fire microbial community dynamics in the boreal bryosphere (the living and dead parts of the feather moss layer on the forest floor, along with the associated biota). We anticipated systematic changes in microbial community structure and growth strategy with increasing time since fire (TSF) and used amplicon pyrosequencing to establish microbial community structure. We also recorded edaphic factors (relating to pH, C and N accumulation) and the physical characteristics of the feather moss layer. The molecular analyses revealed an unexpectedly diverse microbial community. The structure of the community could be largely explained by just two factors, TSF and pH, although the importance of TSF diminished as the forest recovered from disturbance. The microbial communities on the youngest site (TSF = 14 years) were clearly different from older locations (>100 years), suggesting relatively rapid post-fire recovery. A shift towards Proteobacterial taxa on older sites, coupled with a decline in the relative abundance of Acidobacteria, suggested an increase in resource availability with TSF. Saprotrophs dominated the fungal community. Mycorrhizal fungi appeared to decline in abundance with TSF, possibly due to changing N status. Our study provided evidence for the decadal-scale legacy of burning, with implications for boreal forests that are expected to experience more frequent burns over the course of the next century.

Impact of small-scale vegetation structure on tephra layer preservation.

The factors that influence tephra layer taphonomy are poorly understood, but vegetation cover is likely to play a role in the preservation of terrestrial tephra deposits. The impact of vegetation on tephra layer preservation is important because: 1) the morphology of tephra layers could record key characteristics of past land surfaces and 2) vegetation-driven variability in tephra thickness could affect attempts to infer eruption and dispersion parameters. We investigated small- (metre-) scale interactions between vegetation and a thin (<10 cm), recent tephra layer. We conducted surveys of vegetation structure and tephra thickness at two locations which received a similar tephra deposit, but had contrasting vegetation cover (moss vs shrub). The tephra layer was thicker and less variable under shrub cover. Vegetation structure and layer thickness were correlated on the moss site but not under shrub cover, where the canopy reduced the influence of understory vegetation on layer morphology. Our results show that vegetation structure can influence tephra layer thickness on both small and medium (site) scales. These findings suggest that some tephra layers may carry a signal of past vegetation cover. They also have implications for the sampling effort required to reliably estimate the parameters of initial deposits.

The spatial organization and microbial community structure of an epilithic biofilm.

Microbial biofilms are common on lithic surfaces, including stone buildings. However, the ecology of these communities is poorly understood. Few studies have focused on the spatial characteristics of lithobiontic biofilms, despite the fact that spatial structure has been demonstrated to influence ecosystem function (and hence biodegradation) and community diversity. Furthermore, relatively few studies have utilized molecular techniques to characterize these communities, even though molecular methods have revealed unexpected microbial diversity in other habitats. This study investigated (1) the spatial structure and (2) the taxonomic composition of an epilithic biofilm using molecular techniques, namely amplicon pyrosequencing and terminal restriction fragment length polymorphism. Dispersion indices and Mantel correlograms were used to test for the presence of spatial structure in the biofilm. Diversity metrics and rank-abundance distributions (RADs) were also generated. The study revealed spatial structure on a centimetre scale in eukaryotic microbes (fungi and algae), but not the bacteria. Fungal and bacterial communities were highly diverse; algal communities much less so. The RADs were characterized by a distinctive 'hollow' (concave up) profile and long tails of rare taxa. These findings have implications for understanding the ecology of epilithic biofilms and the spatial heterogeneity of stone biodeterioration.

Algal 'greening' and the conservation of stone heritage structures.

In humid, temperate climates, green algae can make a significant contribution to the deterioration of building stone, both through unsightly staining ('greening') and, possibly, physical and chemical transformations. However, very little is known about the factors that influence the deteriorative impact and spatial distribution of green algal biofilms, hindering attempts to model the influence of climate change on building conservation. To address this problem, we surveyed four sandstone heritage structures in Belfast, UK. Our research had two aims: 1) to investigate the relationships between greening and the deterioration of stone structures and 2) to assess the impacts of environmental factors on the distribution of green biofilms. We applied an array of analytical techniques to measure stone properties indicative of deterioration status (hardness, colour and permeability) and environmental conditions related to algal growth (surface and sub-surface moisture, temperature and surface texture). Our results indicated that stone hardness was highly variable but only weakly related to levels of greening. Stone that had been exposed for many years was, on average, darker and greener than new stone of the same type, but there was no correlation between greening and darkening. Stone permeability was higher on 'old', weathered stone but not consistently related to the incidence of greening. However, there was evidence to suggest that thick algal biofilms were capable of reducing the ingress of moisture. Greening was negatively correlated with point measurements of surface temperature, but not moisture or surface texture. Our findings suggested that greening had little impact on the physical integrity of stone; indeed the influence of algae on moisture regimes in stone may have a broadly bioprotective action. Furthermore, the relationship between moisture levels and greening is not straightforward and is likely to be heavily dependent upon temporal patterns in moisture regimes and other, unmeasured, factors such as nutrient supply.

Non-destructive sampling of rock-dwelling microbial communities using sterile adhesive tape.

Building stone provides a habitat for an array of microorganisms, many of which have been demonstrated to have a deleterious effect on the appearance and/or structural integrity of stone masonry. It is essential to understand the composition and structure of stone-dwelling (lithobiontic) microbial communities if successful stone conservation strategies are to be applied, particularly in the face of global environmental change. Ideally, the techniques used to sample such assemblages should be non-destructive due to the sensitive conservation status of many stone buildings. This paper quantitatively assesses the performance of sterile adhesive tape as a non-destructive sampling technique and compares the results of tape sampling with an alternative, destructive, sampling method. We used DNA fingerprinting (TRFLP) to characterise the algal, fungal and bacterial communities living on a stone slab. Our results demonstrate that tape sampling may be used to collect viable quantities of microbial DNA from environmental samples. This technique is ideally suited to the sampling of microbial biofilms, particularly when these communities are dominated by green algae. It provides a good approximation of total community diversity (i.e. the aggregate diversity of epilithic and endolithic communities). Tape sampling is straightforward, rapid and cost effective. When combined with molecular analytical techniques, this sampling method has the potential to make a major contribution to efforts to understand the structure of lithobiontic microbial communities and our ability to predict the response of such communities to future environmental change.