bioRxiv Science⌕ Search

Biology subjects

Griffiths, R. I.

Publications and source records attributed to Griffiths, R. I..

11 recordsLinked to original sources

Soil microenvironment and microbial community composition jointly regulate carbon accrual in agricultural soils

Much of the persistent soil organic carbon (SOC) pool is microbial in origin: microorganisms process plant carbon into biomass and their necromass can associate with mineral surfaces, contributing to long-term carbon persistence. This has generated interest in microbial interventions such as inoculation to restore carbon in degraded croplands, yet their efficacy remains uncertain. The uncertainty reflects a more fundamental, unresolved question: are microbially-mediated carbon transformations governed principally by the composition of the microbial community or by the soil microenvironment? To disentangle these drivers, we conducted a reciprocal microbial community transplant experiment, introducing communities of contrasting origin from locally adjacent grassland and cropland soils into sterilised grassland and cropland soils, and incubating them for eight months with regular organic inputs. This design decouples the inoculum from the microenvironment, allowing their individual and interactive contributions to be quantified. Fungal assembly was influenced more by the inoculum, consistent with dispersal limitation, whereas bacterial assembly was governed more by the microenvironment, consistent with environmental selection. Despite receiving the same organic carbon inputs, grassland and cropland recipient soils showed distinct SOC trajectories, indicating that the soil microenvironment strongly constrained net carbon retention. Within this constraint, community composition also mattered: introducing grassland rather than cropland communities increased fungal diversity and fungal necromass and led to better SOC outcomes, expressed as net gain or reduced loss. These results show that SOC accrual emerges from interactions between the soil microenvironment and microbial community composition, with fungal community assembly particularly associated with necromass accumulation and carbon retention. They highlight the need to consider both soil conditions and microbial community composition when developing strategies to enhance SOC accrual.

ecology↗

Antimicrobial resistance as a signature of soil restoration across a 143-year chronosequence

Restoring agriculturally degraded habitats to species-rich grasslands is a vital conservation objective. During restoration, how the soil resistome matures alongside microbial community composition and function remains unclear. Here, we tested two competing hypotheses: whether the soil resistome matures through a microbial warfare model, in which restoration fosters higher-order biotic interactions, or whether antimicrobial resistance (AMR) is instead driven by the competitive pressures of the high taxonomic richness found in disturbed, eutrophic arable land. Using a unique land-use chronosequence on Salisbury Plain, UK, we investigated the trajectory of ecosystem reassembly following the cessation of agricultural activity. Our results demonstrate that AMR abundance increases significantly with restoration age, reaching a maximum in >143-year-old soils. Aligned with this rise in AMR abundance were significant increases in microbial biomass, dominance and cross-kingdom interaction as the ecosystem matured. This suggests that resistome expansion is not associated with generalised bacterial competition, but by a structural maturation of the microbiome. We observed an order of magnitude increase in biosynthetic potential, dominated by the emergence of streptomycin clusters. This maturation was characterised by a loss of bacterial diversity and a systematic shift towards high eukaryote-to-prokaryote ratios. This reorientation mirrors the expansion of a core resistome comprised of ancient, intrinsic mechanisms, such as MFS efflux pumps and RbpA target protection, in older soils. We demonstrate that endogenous AMR is a hallmark of healthy, restored soil ecosystems rather than a marker of anthropogenic degradation, positioning the resistome as bio-indicator of edaphic restoration success within calcareous soils.

microbiology↗

Taxonomic filtering accompanies functional expansion during long-term soil restoration

The restoration of species-rich calcareous grasslands is a critical conservation objective, yet the recovery of the invisible below-ground microbiome remains poorly quantified compared to above-ground vegetation. Using a unique 143-year land-use chronosequence on Salisbury Plain, UK, we investigated the trajectory of ecosystem reassembly across arable, regenerating (23 and 67 years), and ancient grasslands. By integrating vegetation surveys with soil physiochemistry, microbial profiling, and shotgun metagenomics, we identified a profound functional decoupling between floral and edaphic recovery. While vegetation diversity recovered relatively rapidly, approaching saturation within 23-67 years, soil properties exhibited persistent legacy effects and slow convergence. Bacterial richness decreased with restoration age, reflecting a transition from disturbance-adapted copiotrophs in arable soils to a specialised, oligotrophic community in ancient sites. This taxonomic contraction was conversely matched by an expansion in functional potential, driven by the emergence of specific taxa (e.g., Microthrixaceae, Aquihabitans sp.) and metabolic pathways associated with complex carbon cycling and stress tolerance. Crucially, the soil ecosystem did not reach equilibrium even after 67 years, characterised by persistent legacy phosphorus and a slow accumulation of soil organic matter. These findings suggest that passive regeneration alone may be insufficient for full soil functional recovery, and that strategies targeting microbial assembly and long-term carbon dynamics warrant further evaluation.

ecology↗

Environmental filtering shapes divergent bacterial strategies and genomic traits across soil niches

Soil pH is a predominant factor in structuring microbial communities; however, its role in shaping microbial life-history traits across large spatial scales remains underexplored. Here, we hypothesised that bacterial ubiquity, or niche breadth, across a diverse collection of soils is linked to genomic traits. We leveraged a national-scale survey of UK soils (the Countryside Survey) and 16S rRNA gene sequencing data with trait annotations (estimated genome size, coding density, and rRNA operon copy number) to examine trait-environment-niche breadth relationships. Our analyses revealed that soil pH was the dominant environmental driver of niche classification and bacterial community traits along the niche range. Low pH soils (pH <5.5) hosted ubiquitous taxa with larger genome sizes, lower coding densities and lower rRNA copy numbers, implying slower growing taxa with higher genetic facilities. Mildly acidic soils (pH 5.5 to 7) favour higher rRNA copy numbers, intermediate genome sizes and moderate coding densities. Alkaline soils (pH >7) feature communities with the smallest niche range, smallest genomes and highest coding densities. Here, specialisation occurs through streamlining with simpler, smaller genomes favoured. We found that generalist taxa were widespread across the pH range, becoming dominant under acidic conditions, while taxa adapted to higher pH were comparatively scarce in their distribution. These findings identify soil pH as a key physiological filter that aligns microbial genomic traits and ecological strategies across landscapes. By extending prior site-specific results to a broad-scale context, our study highlights how trait-based metrics can predict microbial responses to soil conditions, with implications for understanding ecosystem carbon cycling and informing land management practices aimed at sustaining soil health in the future.

microbiology↗

Deciphering landscape-scale plant cover and biodiversity from soil eDNA

Biodiversity surveys are critical for detecting environmental change; however, undertaking them at scale and capturing all available diversity through observation is challenging and costly. This study evaluated the potential of soil-extracted eDNA to describe plant communities and compared these findings to traditional, observation-based, field surveys. We analysed 789 soil samples using high-throughput amplicon sequencing and compared DNA-based diversity metrics, indicator taxa, predicted vegetation class, and plant cover in a comparison with co-located field survey data. The results indicated that taxonomically aggregated (genus) eDNA-derived data, while showing slightly reduced Shannons diversity scores, yielded remarkably similar overall richness and composition estimates. However, the DNA indicator taxa and predictive power for vegetation community classification were also lower overall than those recorded by the field survey. However, in many cases plant cover could be inferred from amplicon abundance data with some accuracy despite widely differing scales of sampling - 0.25 g crumb of soil versus a 1 m2 quadrat. Overall, results from eDNA demonstrated lower sensitivity but were broadly in accordance with traditional surveys, with our findings revealing comparable taxonomic resolution at the genus level. We demonstrate the potential and limitations of a simple molecular method to inform landscape-scale plant biodiversity surveys, a vital tool in the monitoring of land use and environmental change.

molecular biology↗

Land use effects on soil microbiome composition and traits with consequences for its ecosystem carbon use efficiency

The soil microbiome determines the fate of belowground inputs of plant fixed carbon. The shifts in soil properties caused by changes in land use leads to modifications in microbiome structure and function, resulting in either loss or gain of soil organic carbon (SOC). Soil pH is the primary factor regulating microbiome characteristics leading to distinct pathways of microbial carbon cycling, but the underlying mechanisms remain understudied. Here, the taxa-trait relationships behind the variable fate of SOC were investigated across two temperate paired land use intensity contrasts with differing soil pH using metaproteomics, metabarcoding and a 13C labelled litter decomposition experiment. 13C incorporation into microbial biomass increased with land use intensification in low pH soils but decreased in high pH soils, impacting ecosystem carbon use efficiency (CUE) in opposing directions. Reduction in biosynthesis traits across land use intensity contrasts was due to increased abundance of proteins linked to resource acquisition and stress tolerance. These community-level trait trade-offs were underpinned by land use intensification-induced changes in dominant taxa with distinct traits. These trait changes alter the balance of decomposition and stabilisation of carbon in soil through divergent pH-controlled pathways. In low pH soils, land use intensification alleviates microbial abiotic stress resulting in increased CUE but promotes decomposition and SOC loss. In contrast, in high pH soils, land use intensification increases microbial physiological constraints and decreases CUE, leading to reduced necromass build-up and SOC stabilisation. We demonstrate how microbial CUE can be decoupled from SOC highlighting the need for its careful consideration in predicting or managing SOC storage for soil health and climate change mitigation.

ecology↗

Soil bacterial and fungal communities show within field heterogeneity that varies by land management and distance metric

Increasing interest in the use of microbial metrics to evaluate soil health raises the issue of how fine-scale heterogeneity can affect microbial community measurements. Here we analyse bacterial and fungal communities of over 100 soil samples across 17 pasture farms and evaluate beta diversity at different scales. We find large variation in microbial communities between different points in the same field, and if Aitchison distance is used we find that within-field variation is as high as between-farm variation. However, if Bray-Curtis or Jaccard distance are used this variation is partially explained by differences in soil pH and vegetation and is higher under mob grazing for fungi. Hence, field scale variation in microbial communities can impact the evaluation of soil health.

ecology↗

Pasture age impacts soil fungal composition while bacteria respond to soil chemistry

Pasture is a globally important managed habitat providing both food and income. The way in which it is managed leads to a wide range of impacts on soil microbial communities and associated soil health. While there have been several studies comparing pasture farming to other forms of land use, we still have limited understanding of how the soil microbial communities vary between pasture farms and according to management practices. Here we present the results of a field survey across 56 UK livestock farms that are managed by members of the Pasture fed Livestock Association, using amplicon sequencing of the 16S and ITS regions to characterise the soil bacterial and fungal community within fields that have been under pasture for differing durations. We show that grazing management intensity has only limited effects upon microbial community structure, while the duration of pasture since ploughing (ranging from 1 year to over 100 years) impacted the fungal community structure. The impact of management duration was conditional upon soil physicochemical properties, particularly pH. Plant community effects on upon soil bacterial and fungal composition appear to also interact with the soil chemistry, highlighting the importance of plant-soil interactions in determining microbial community structure. Analyses of microbial indicators revealed proportionally more fungal taxa that responded to multiple ecosystem health associated properties than bacterial taxa. We also identified several fungal taxa that both acted as indicators of soil health related properties within our dataset and showed differentiation between grassland types in a national survey, indicating the generality of some fungal indicators to the national level. Members of the Agaricomycetes were associated with multiple indicators of soil health. Our results show the importance of maintaining grassland for the development of plant-soil interactions and microbial community structure with concomitant effects on soil and general ecosystem health. HighlightsO_LISoil bacteria and fungi from >50 pastures were analysed using DNA metabarcoding C_LIO_LIDuration of pasture since ploughing impacted fungal community composition C_LIO_LIBacteria were more associated with soil physicochemical properties than fungi C_LIO_LIPlant effects on soil microbes were through interactions with soil chemistry C_LIO_LIMicrobial indicators of soil health were disproportionately fungal taxa C_LI

ecology↗

The effect of plant-derived carbon on rhizospheric microbial communities decomposing different litter types and nutrient return

Interactions between plants and microorganisms strongly affect ecosystem functioning as processes of plant productivity, litter decomposition and nutrient cycling are controlled by both organisms. Though two-sided interactions between plants and microorganisms and between microorganisms and litter decomposition are areas of major scientific research, our understanding of the three-sided interactions of plant-derived carbon flow into the soil microbial community and their follow-on effects on ecosystem processes like litter decomposition and plant nutrient uptake remains limited. Therefore, we performed a greenhouse experiment with two plant communities differing in their ability to associate with arbuscular mycorrhizal fungi (AMF). By applying a 13CO2 pulse label to the plant communities and adding various 15N labelled substrate types to ingrowth cores, we simultaneously traced the flow of plant-derived carbon into soil microbial communities and the return of mineralized nitrogen back to the plant communities. We observed that net 13C assimilation by the rhizosphere microbial communities and their community composition not only depended on plant-AMF association but also type of substrate being decomposed. AMF-association resulted in lower net 13C investment into the decomposer community than absence of the association for similar 15N uptake. This effect was driven by a reduced carbon flow to fungal and bacterial saprotrophs and a simultaneous increase of carbon flow to AMF. Additionally, in presence of AMF association CN flux also depended on the type of substrate being decomposed. Lower net 13C assimilation was observed for decomposition of plant-derived and microorganism-derived substrates whereas opposite was true for inorganic nitrogen. Interestingly, the decomposer communities assembled in the rhizosphere were structured by both the plant community and substrate amendments which suggests existence of functional overlap between the two soil contexts. Moreover, we present preliminary evidence that AMF association helps plants access nutrients that are locked in bacterial and plant necromass at a lower carbon cost. Therefore, we conclude that a better understanding of ecosystem processes like decomposition can only be achieved when the whole plant-microorganism-litter context is investigated.

microbiology↗

Soil microbial communities with greater investment in resource acquisition have lower growth yield

Resource acquisition and growth yield are fundamental traits of microorganisms that have consequences for ecosystem functioning. However, there is a lack of empirical observations linking these traits. Using a landscape-scale survey of temperate near-neutral pH soils, we show tradeoffs in key community-level parameters linked to these traits. Increased investment into extracellular enzymes was associated with reduced growth yield; this reduction was linked more to carbon than nitrogen acquisition enzymes suggesting smaller stoichiometric constraints on community metabolism in examined soils.

ecology↗

Bacterial physiological adaptations to contrasting edaphic conditions identified using landscape scale metagenomics

Environmental factors relating to soil pH are widely known to be important in structuring soil bacterial communities, yet the relationship between taxonomic community composition and functional diversity remains to be determined. Here, we analyze geographically distributed soils spanning a wide pH gradient and assess the functional gene capacity within those communities using whole genome metagenomics. Low pH soils consistently had fewer taxa (lower alpha and gamma diversity), but only marginal reductions in functional alpha diversity and equivalent functional gamma diversity. However, coherent changes in the relative abundances of annotated genes between pH classes were identified; with functional profiles clustering according to pH independent of geography. Differences in gene abundances were found to reflect survival and nutrient acquisition strategies, with organic-rich acidic soils harboring a greater abundance of cation efflux pumps, C and N direct fixation systems and fermentation pathways indicative of anaerobiosis. Conversely, high pH soils possessed more direct transporter-mediated mechanisms for organic C and N substrate acquisition. These findings show that bacterial functional versatility may not be constrained by taxonomy, and we further identify the range of physiological adaptations required to exist in soils of varying nutrient availability and edaphic conditions.

microbiology↗