Secondary successional trajectories of structural and catabolic bacterial communities in oil‐polluted soil planted with hybrid poplar

Poplars have widely been used for rhizoremediation of a broad range of organic contaminants for the past two decades. Still, there is a knowledge gap regarding the rhizosphere‐associated bacterial communities of poplars and their dynamics during the remediation process. It is envisaged that a detailed understanding of rhizosphere‐associated microbial populations will greatly contribute to a better design and implementation of rhizoremediation. To investigate the long‐term succession of structural and catabolic bacterial communities in oil‐polluted soil planted with hybrid poplar, we carried out a 2‐year field study. Hybrid aspen (Populus tremula × Populus tremuloides) seedlings were planted in polluted soil excavated from an accidental oil‐spill site. Vegetated and un‐vegetated soil samples were collected for microbial community analyses at seven different time points during the course of 2 years and sampling time points were chosen to cover the seasonal variation in the boreal climate zone. Bacterial community structure was accessed by means of 16S rRNA gene amplicon pyrosequencing, whereas catabolic diversity was monitored by pyrosequencing of alkane hydroxylase and extradiol dioxygenase genes. We observed a clear succession of bacterial communities on both structural and functional levels from early to late‐phase communities. Sphingomonas type extradiol dioxygenases and alkane hydroxylase homologs of Rhodococcus clearly dominated the early‐phase communities. The high‐dominance/low‐diversity functional gene communities underwent a transition to low‐dominance/high‐diversity communities in the late phase. These results pointed towards increased catabolic capacities and a change from specialist to generalist strategy of bacterial communities during the course of secondary succession.     

Contrasting primary successional trajectories of fungi and bacteria in retreating glacier soils

Early community assembly of soil microbial communities is essential for pedogenesis and development of organic legacies. We examined fungal and bacterial successions along a well‐established temperate glacier forefront chronosequence representing ~70 years of deglaciation to determine community assembly. As microbial communities may be heavily structured by establishing vegetation, we included nonvegetated soils as well as soils from underneath four plant species with differing mycorrhizal ecologies (Abies lasiocarpa, ectomycorrhizal; Luetkea pectinata, arbuscular mycorrhizal; Phyllodoce empetriformis, ericoid mycorrhizal; Saxifraga ferruginea, nonmycorrhizal). Our main objectives were to contrast fungal and bacterial successional dynamics and community assembly as well as to decouple the effects of plant establishment and time since deglaciation on microbial trajectories using high‐throughput sequencing. Our data indicate that distance from glacier terminus has large effects on biomass accumulation, community membership, and distribution for both fungi and bacteria. Surprisingly, presence of plants rather than their identity was more important in structuring bacterial communities along the chronosequence and played only a very minor role in structuring the fungal communities. Further, our analyses suggest that bacterial communities may converge during assembly supporting determinism, whereas fungal communities show no such patterns. Although fungal communities provided little evidence of convergence in community structure, many taxa were nonrandomly distributed across the glacier foreland; similar taxon‐level responses were observed in bacterial communities. Overall, our data highlight differing drivers for fungal and bacterial trajectories during early primary succession in recently deglaciated soils.     

Bacterial Community Succession in Natural River Biofilm Assemblages

Temporal bacterial community changes in river biofilms were studied using 16S rRNA gene-based polymerase chain reaction–denaturing gradient gel electrophoresis (DGGE) followed by sequence analysis. Naturally occurring biofilms were sampled in 2001 during an undisturbed 7-month low-water period in the River Garonne (SW France). During the sampling period epilithic biomass exhibited a particular pattern: two 3-month periods of accumulation that resulted in two peaks in summer and fall, each at about 25 g ash-free dry mass per square meter. Bacterial community DGGE profiles differed between the summer and fall biomass peaks and shared only 30% common operational taxonomic units (OTUs), suggesting the influence of seasonal factors on these communities. During the second biomass accrual phase, bacterial richness and the appearance of new OTUs fitted a conceptual model of bacterial biofilm succession. During succession, five OTUs (corresponding to Dechloromonas sp., Nitrospira sp., and three different Spirosoma spp.) exhibited particular patterns and were present only during clearly defined successional stages, suggesting differences in life-history strategies for epilithic bacteria. Co-inertia analysis of DGGE banding patterns and physical–chemical data showed a significant relationship between community structure and environmental conditions suggesting that bacterial communities were mainly influenced by seasonal changes (temperature, light) and hydrodynamic stability. Within the periods of stability, analysis of environmental variables and community patterns showed the dominant influence of time and maturation on bacterial community structure. Thus, succession in these naturally occurring epilithic biofilm assemblages appears to occur through a combination of allogenic (seasonal) and autogenic changes.     

Bacterial Succession on the Leaf Surface: A Novel System for Studying Successional Dynamics

Succession is a widely studied process in plant and animal systems, but succession in microbial communities has received relatively little attention despite the ubiquity of microorganisms in natural habitats. One important microbial habitat is the phyllosphere, or leaf surface, which harbors large, diverse populations of bacteria and offers unique opportunities for the study of succession and temporal community assembly patterns. To explore bacterial community successional patterns, we sampled phyllosphere communities on cottonwood (Populus deltoides) trees multiple times across the growing season, from leaf emergence to leaf fall. Bacterial community composition was highly variable throughout the growing season; leaves sampled as little as a week apart were found to harbor significantly different communities, and the temporal variability on a given tree exceeded the variability in community composition between individual trees sampled on a given day. The bacterial communities clearly clustered into early-, mid-, and late-season clusters, with early- and late-season communities being more similar to each other than to the mid-season communities, and these patterns appeared consistent from year to year. Although we observed clear and predictable changes in bacterial community composition during the course of the growing season, changes in phyllosphere bacterial diversity were less predictable. We examined the species–time relationship, a measure of species turnover rate, and found that the relationship was fundamentally similar to that observed in plant and invertebrate communities, just on a shorter time scale. The temporal dynamics we observed suggest that although phyllosphere bacterial communities have high levels of phylogenetic diversity and rapid turnover rates, these communities follow predictable successional patterns from season to season.     

Influence of corn,switchgrass, and prairie cropping systems on soil microbial communities in the upper Midwest of the United States

Because soil microbes drive many of the processes underpinning ecosystem services provided by soils, understanding how cropping systems affect soil microbial communities is important for productive and sustainable management. We characterized and compared soil microbial communities under restored prairie and three potential cellulosic biomass crops (corn, switchgrass, and mixed prairie grasses) in two spatial experimental designs – side‐by‐side plots where plant communities were in their second year since establishment (i.e., intensive sites) and regionally distributed fields where plant communities had been in place for at least 10 years (i.e., extensive sites). We assessed microbial community structure and composition using lipid analysis, pyrosequencing of rRNA genes (targeting fungi, bacteria, archaea, and lower eukaryotes), and targeted metagenomics of nifH genes. For the more recently established intensive sites, soil type was more important than plant community in determining microbial community structure, while plant community was the more important driver of soil microbial communities for the older extensive sites where microbial communities under corn were clearly differentiated from those under switchgrass and restored prairie. Bacterial and fungal biomasses, especially biomass of arbuscular mycorrhizal fungi, were higher under perennial grasses and restored prairie, suggesting a more active carbon pool and greater microbial processing potential, which should be beneficial for plant acquisition and ecosystem retention of carbon, water, and nutrients.     

Microbial community composition but not diversity changes along succession in arctic sand dunes

The generality of increasing diversity of fungi and bacteria across arctic sand dune succession was tested. Microbial communities were examined by high‐throughput sequencing of 16S rRNA genes (bacteria) and internal transcribed spacer (ITS) regions (fungi). We studied four microbial compartments (inside leaf, inside root, rhizosphere and bulk soil) and characterized microbes associated with a single plant species (Deschampsia flexuosa) across two sand dune successional stages (early and late). Bacterial richness increased across succession in bulk soil and leaf endosphere. In contrast, soil fungal richness remained constant while root endosphere fungal richness increased across succession. There was, however, no significant difference in Shannon diversity indices between early and late successional stage in any compartment. There was a significant difference in the composition of microbial communities between early and late successional stage in all compartments, although the major microbial OTUs were shared between early and late successional stage. Co‐occurrence network analysis revealed successional stage‐specific microbial groups. There were more co‐occurring modules in early successional stage than in late stage. Altogether, these results emphasize that succession strongly affects distribution of microbial species, but not microbial diversity in arctic sand dune ecosystem and that fungi and bacteria may not follow the same successional trajectories.     

Elevated success of multispecies bacterial invasions impacts community composition during ecological succession

Successful microbial invasions are determined by a species’ ability to occupy a niche in the new habitat whilst resisting competitive exclusion by the resident community. Despite the recognised importance of biotic factors in determining the invasiveness of microbial communities, the success and impact of multiple concurrent invaders on the resident community has not been examined. Simultaneous invasions might have synergistic effects, for example if resident species need to exhibit divergent phenotypes to compete with the invasive populations. We used three phylogenetically diverse bacterial species to invade two compositionally distinct communities in a controlled, naturalised in vitro system. By initiating the invader introductions at different stages of succession, we could disentangle the relative importance of resident community structure, invader diversity and time pre‐invasion. Our results indicate that multiple invaders increase overall invasion success, but do not alter the successional trajectory of the whole community.     

Environmental degradation results in contrasting changes in the assembly processes of stream bacterial and fungal communities

Environmental degradation may have strong effects on community assembly processes. We examined the assembly of bacterial and fungal communities in anthropogenically altered and near‐pristine streams. Using pyrosequencing of bacterial and fungal DNA from decomposed alder Alnus incana leaves, we specifically examined if environmental degradation deterministically decreases or increases the compositional turnover of bacterial and fungal communities. Our results showed that near‐pristine streams and anthropogenically altered streams supported distinct fungal and bacterial communities. The mechanisms assembling these communities were different in near‐pristine and altered environments. Environmental disturbance homogenized bacterial communities, whereas fungal communities were more dissimilar in disturbed sites than in near‐pristine sites. Compositional variation of both bacteria and fungi was related to water chemistry variables in disturbed sites, further implying the influence of environmental degradation on community assembly. Bacterial and fungal communities in near‐pristine streams were weakly controlled by environmental factors, suggesting that the relative importance of niche‐based versus neutral processes in assembling microbial communities may strongly depend on the spatial scale and local environmental context. Our results thus suggest that environmental degradation may strongly affect the composition and β‐diversity of stream microbial communities colonizing leaf litter, and that the direction of the change can be different between bacteria and fungi. A better understanding of the environmental tolerances of microbes and the mechanisms assembling microbial communities in natural environmental settings is needed to predict how environmental alteration is likely to affect microbial communities.     

Changes in northern Gulf of Mexico sediment bacterial and archaeal communities exposed to hypoxia

Biogeochemical changes in marine sediments during coastal water hypoxia are well described, but less is known about underlying changes in microbial communities. Bacterial and archaeal communities in Louisiana continental shelf (LCS) hypoxic zone sediments were characterized by pyrosequencing 16S rRNA V4‐region gene fragments obtained by PCR amplification of community genomic DNA with bacterial‐ or archaeal‐specific primers. Duplicate LCS sediment cores collected during hypoxia had higher concentrations of Fe(II), and dissolved inorganic carbon, phosphate, and ammonium than cores collected when overlying water oxygen concentrations were normal. Pyrosequencing yielded 158 686 bacterial and 225 591 archaeal sequences from 20 sediment samples, representing five 2‐cm depth intervals in the duplicate cores. Bacterial communities grouped by sampling date and sediment depth in a neighbor‐joining analysis using Chao–Jaccard shared species values. Redundancy analysis indicated that variance in bacterial communities was mainly associated with differences in sediment chemistry between oxic and hypoxic water column conditions. Gammaproteobacteria (26.5%) were most prominent among bacterial sequences, followed by Firmicutes (9.6%), and Alphaproteobacteria (5.6%). Crenarchaeotal, thaumarchaeotal, and euryarchaeotal lineages accounted for 57%, 27%, and 16% of archaeal sequences, respectively. In Thaumarchaeota Marine Group I, sequences were 96–99% identical to the Nitrosopumilus maritimus SCM1 sequence, were highest in surficial sediments, and accounted for 31% of archaeal sequences when waters were normoxic vs. 13% of archaeal sequences when waters were hypoxic. Redundancy analysis showed Nitrosopumilus‐related sequence abundance was correlated with high solid‐phase Fe(III) concentrations, whereas most of the remaining archaeal clusters were not. In contrast, crenarchaeotal sequences were from phylogenetically diverse lineages, differed little in relative abundance between sampling times, and increased to high relative abundance with sediment depth. These results provide further evidence that marine sediment microbial community composition can be structured according to sediment chemistry and suggest the expansion of hypoxia in coastal waters may alter sediment microbial communities involved in carbon and nitrogen cycling.     

Primary succession of Bistorta vivipara (L.) Delabre (Polygonaceae) root‐associated fungi mirrors plant succession in two glacial chronosequences

Glacier chronosequences are important sites for primary succession studies and have yielded well‐defined primary succession models for plants that identify environmental resistance as an important determinant of the successional trajectory. Whether plant‐associated fungal communities follow those same successional trajectories and also respond to environmental resistance is an open question. In this study, 454 amplicon pyrosequencing was used to compare the root‐associated fungal communities of the ectomycorrhizal (ECM) herb Bistorta vivipara along two primary succession gradients with different environmental resistance (alpine versus arctic) and different successional trajectories in the vascular plant communities (directional replacement versus directional non‐replacement). At both sites, the root‐associated fungal communities were dominated by ECM basidiomycetes and community composition shifted with increasing time since deglaciation. However, the fungal community's successional trajectory mirrored the pattern observed in the surrounding plant community at both sites: the alpine site displayed a directional‐replacement successional trajectory, and the arctic site displayed a directional‐non‐replacement successional trajectory. This suggests that, like in plant communities, environmental resistance is key in determining succession patterns in root‐associated fungi. The need for further replicated study, including in other host species, is emphasized.     

Do bacterial and fungal communities assemble differently during primary succession?

High‐throughput sequencing technologies are now allowing us to study patterns of community assembly for diverse microbial assemblages across environmental gradients and during succession. Here we discuss potential explanations for similarities and differences in bacterial and fungal community assembly patterns along a soil chronosequence in the foreland of a receding glacier. Although the data are not entirely conclusive, they do indicate that successional trajectories for bacteria and fungi may be quite different. Recent empirical and theoretical studies indicate that smaller microbes (like most bacteria) are less likely to be dispersal limited than are larger microbes – which could result in a more deterministic community assembly pattern for bacteria during primary succession. Many bacteria are also better adapted (than are fungi) to life in barren, early‐successional sediments in that some can fix nitrogen and carbon from the atmosphere – traits not possessed by any fungi. Other differences between bacteria and fungi are discussed, but it is apparent from this and other recent studies of microbial succession that we are a long way from understanding the mechanistic underpinnings of microbial community assembly during ecosystem succession. We especially need a better understanding of global and regional patterns of microbial dispersal and what environmental factors control the development of microbial communities in complex natural systems.     

Spatial structure in the “Plastisphere”: Molecular resources for imaging microscopic communities on plastic marine debris

Plastic marine debris (PMD) affects spatial scales of life from microbes to whales. However, understanding interactions between plastic and microbes in the “Plastisphere”—the thin layer of life on the surface of PMD—has been technology‐limited. Research into microbe–microbe and microbe–substrate interactions requires knowledge of community phylogenetic composition but also tools to visualize spatial distributions of intact microbial biofilm communities. We developed a CLASI‐FISH (combinatorial labelling and spectral imaging – fluorescence in situ hybridization) method using confocal microscopy to study Plastisphere communities. We created a probe set consisting of three existing phylogenetic probes (targeting all Bacteria, Alpha‐, and Gammaproteobacteria) and four newly designed probes (targeting Bacteroidetes, Vibrionaceae, Rhodobacteraceae and Alteromonadaceae) labelled with a total of seven fluorophores and validated this probe set using pure cultures. Our nested probe set strategy increases confidence in taxonomic identification because targets are confirmed with two or more probes, reducing false positives. We simultaneously identified and visualized these taxa and their spatial distribution within the microbial biofilms on polyethylene samples in colonization time series experiments in coastal environments from three different biogeographical regions. Comparing the relative abundance of 16S rRNA gene amplicon sequencing data with cell‐count abundance data retrieved from the microscope images of the same samples showed a good agreement in bacterial composition. Microbial communities were heterogeneous, with direct spatial relationships between bacteria, cyanobacteria and eukaryotes such as diatoms but also micro‐metazoa. Our research provides a valuable resource to investigate biofilm development, succession and associations between specific microscopic taxa at micrometre scales.     

Life in leaf litter: novel insights into community dynamics of bacteria and fungi during litter decomposition

Microorganisms play a crucial role in the biological decomposition of plant litter in terrestrial ecosystems. Due to the permanently changing litter quality during decomposition, studies of both fungi and bacteria at a fine taxonomic resolution are required during the whole process. Here we investigated microbial community succession in decomposing leaf litter of temperate beech forest using pyrotag sequencing of the bacterial 16S and the fungal internal transcribed spacer (ITS) rRNA genes. Our results reveal that both communities underwent rapid changes. Proteobacteria, Actinobacteria and Bacteroidetes dominated over the entire study period, but their taxonomic composition and abundances changed markedly among sampling dates. The fungal community also changed dynamically as decomposition progressed, with ascomycete fungi being increasingly replaced by basidiomycetes. We found a consistent and highly significant correlation between bacterial richness and fungal richness (R = 0.76, P < 0.001) and community structure (R_Mantel = 0.85, P < 0.001), providing evidence of coupled dynamics in the fungal and bacterial communities. A network analysis highlighted nonrandom co‐occurrences among bacterial and fungal taxa as well as a shift in the cross‐kingdom co‐occurrence pattern of their communities from the early to the later stages of decomposition. During this process, macronutrients, micronutrients, C:N ratio and pH were significantly correlated with the fungal and bacterial communities, while bacterial richness positively correlated with three hydrolytic enzymes important for C, N and P acquisition. Overall, we provide evidence that the complex litter decay is the result of a dynamic cross‐kingdom functional succession.     

A closer look at the species behind abundance–occupancy relationships

Guedo & Lamb ( 2013 ), in this issue of the Journal of Vegetation Science, used a 35‐yr data series from two prairie communities to show that abundance–occupancy relationships change over time. Scrutinizing the details behind this finding, they show that species groups follow different trajectories during succession after disturbance. These results will inspire further species‐level studies unraveling mechanisms behind abundance–occupancy relationships.     

Nutrient Addition Dramatically Accelerates Microbial Community Succession

The ecological mechanisms driving community succession are widely debated, particularly for microorganisms. While successional soil microbial communities are known to undergo predictable changes in structure concomitant with shifts in a variety of edaphic properties, the causal mechanisms underlying these patterns are poorly understood. Thus, to specifically isolate how nutrients – important drivers of plant succession – affect soil microbial succession, we established a full factorial nitrogen (N) and phosphorus (P) fertilization plot experiment in recently deglaciated (∼3 years since exposure), unvegetated soils of the Puca Glacier forefield in Southeastern Peru. We evaluated soil properties and examined bacterial community composition in plots before and one year after fertilization. Fertilized soils were then compared to samples from three reference successional transects representing advancing stages of soil development ranging from 5 years to 85 years since exposure. We found that a single application of +NP fertilizer caused the soil bacterial community structure of the three-year old soils to most resemble the 85-year old soils after one year. Despite differences in a variety of soil edaphic properties between fertilizer plots and late successional soils, bacterial community composition of +NP plots converged with late successional communities. Thus, our work suggests a mechanism for microbial succession whereby changes in resource availability drive shifts in community composition, supporting a role for nutrient colimitation in primary succession. These results suggest that nutrients alone, independent of other edaphic factors that change with succession, act as an important control over soil microbial community development, greatly accelerating the rate of succession.     

Convergence and divergence in a long‐term old‐field succession: the importance of spatial scale and species abundance

Whether plant communities in a given region converge towards a particular stable state during succession has long been debated, but rarely tested at a sufficiently long time scale. By analysing a 50‐year continuous study of post‐agricultural secondary succession in New Jersey, USA, we show that the extent of community convergence varies with the spatial scale and species abundance classes. At the larger field scale, abundance‐based dissimilarities among communities decreased over time, indicating convergence of dominant species, whereas incidence‐based dissimilarities showed little temporal tend, indicating no sign of convergence. In contrast, plots within each field diverged in both species composition and abundance. Abundance‐based successional rates decreased over time, whereas rare species and herbaceous plants showed little change in temporal turnover rates. Initial abandonment conditions only influenced community structure early in succession. Overall, our findings provide strong evidence for scale and abundance dependence of stochastic and deterministic processes over old‐field succession.     

Distinct successional patterns and processes of free-living and particle-attached bacterial communities throughout a phytoplankton bloom

1. Understanding the successional patterns of microbial communities during a phytoplankton bloom is crucial for predicting the compositional and functional stability of lake ecosystems in response to the disturbance of a bloom. Previous studies on bacterial communities associated with blooms have rarely studied the dynamics of these communities. The successional patterns of bacterial communities within different micro-habitats (i.e. water column versus particles) and mechanisms that shape these communities that differ in composition and structure remain unclear.
2. We selected a eutrophic urban lake to investigate the succession of bacterial communities during a bloom. We divided the bacterial communities into free-living (FL) and particle-attached (PA) groups based on their different lifestyles. The amplicon-based 16S rRNA gene high-throughput sequencing technology was used to obtain bacterial community composition and phylogenetic structure.
3. Our study showed distinct successional patterns between FL and PA bacterial communities, and the two bacterial lifestyles showed different responses and resilience to the bloom, in terms of diversity and relative abundance of bacterial taxa. Alpha-diversity of the PA bacterial community decreased during the bloom, whereas that of the FL bacterial community increased. More taxa in the FL bacterial community showed resilience after the disturbance than in the PA bacterial community.
4. The influence of phytoplankton blooms on the assembly of the bacterial community can be viewed as niche selection that led to the decrease in the relative importance of stochastic processes in shaping both FL and PA bacterial communities. This study shows the ecological significance of the bacterial community response to bloom events in lakes. It also shows that assembly processes differ for bacterial communities that have different lifestyles in lake ecosystems disturbed by phytoplankton blooms.

     

History matters: Heterotrophic microbial community structure and function adapt to multiple stressors

Ecosystem functions in streams (e.g., microbially mediated leaf litter breakdown) are threatened globally by the predicted agricultural intensification and its expansion into pristine areas, which is associated with increasing use of fertilizers and pesticides. However, the ecological consequences may depend on the disturbance history of microbial communities. To test this, we assessed the effects of fungicides and nutrients (four levels each) on the structural and functional resilience of leaf‐associated microbial communities with differing disturbance histories (pristine vs. previously disturbed) in a 2 × 4 × 4‐factorial design (n = 6) over 21 days. Microbial leaf breakdown was assessed as a functional variable, whereas structural changes were characterized by the fungal community composition, species richness, biomass, and other factors. Leaf breakdown by the pristine microbial community was reduced by up to 30% upon fungicide exposure compared with controls, whereas the previously disturbed microbial community increased leaf breakdown by up to 85%. This significant difference in the functional response increased in magnitude with increasing nutrient concentrations. A pollution‐induced community tolerance in the previously disturbed microbial community, which was dominated by a few species with high breakdown efficacies, may explain the maintained function under stress. Hence, the global pressure on pristine ecosystems by agricultural expansion is expected to cause a modification in the structure and function of heterotrophic microbial communities, with microbially mediated leaf litter breakdown likely becoming more stable over time as a consequence of fungal community adaptions.