Alex J. Dumbrell

Relative roles of niche and neutral processes in structuring a soil microbial community

Most attempts to identify the processes that structure natural communities have focused on conspicuous macroorganisms whereas the processes responsible for structuring microbial communities remain relatively unknown. Two main theories explaining these processes have emerged; niche theory, which highlights the importance of deterministic processes, and neutral theory, which focuses on stochastic processes. We examined whether neutral or niche-based mechanisms best explain the composition and structure of communities of a functionally important soil microbe, the arbuscular mycorrhizal (AM) fungi. Using molecular techniques, we surveyed AM fungi from 425 individual plants of 28 plant species along a soil pH gradient. There was evidence that both niche and neutral processes structured this community. Species abundances fitted the zero-sum multinomial distribution and there was evidence of dispersal limitation, both indicators of neutral processes. However, we found stronger support that niche differentiation based on abiotic soil factors, primarily pH, was structuring the AM fungal community. Host plant species affected AM fungal community composition negligibly compared to soil pH. We conclude that although niche partitioning was the primary mechanism regulating the composition and diversity of natural AM fungal communities, these communities are also influenced by stochastic-neutral processes. This study represents one of the most comprehensive investigations of community-level processes acting on soil microbes; revealing a community that although influenced by stochastic processes, still responded in a predictable manner to a major abiotic niche axis, soil pH. The strong response to environmental factors of this community highlights the susceptibility of soil microbes to environmental change.

Distinct seasonal assemblages of arbuscular mycorrhizal fungi revealed by massively parallel pyrosequencing

• Understanding the dynamics of rhizosphere microbial communities is essential for predicting future ecosystem function, yet most research focuses on either spatial or temporal processes, ignoring combined spatio-temporal effects. • Using pyrosequencing, we examined the spatio-temporal dynamics of a functionally important community of rhizosphere microbes, the arbuscular mycorrhizal (AM) fungi. We sampled AM fungi from plant roots growing in a temperate grassland in a spatially explicit manner throughout a year. • Ordination analysis of the AM fungal assemblages revealed significant temporal changes in composition and structure. Alpha and beta diversity tended to be negatively correlated with the climate variables temperature and sunshine hours. Higher alpha diversity during colder periods probably reflects more even competitive interactions among AM fungal species under limited carbon availability, a conclusion supported by analysis of beta diversity which highlights how resource limitation may change localized spatial dynamics. • Results reveal distinct AM fungal assemblages in winter and summer at this grassland site. A seasonally changing supply of host-plant carbon, reflecting changes in temperature and sunshine hours, may be the driving force in regulating the temporal dynamics of AM fungal communities. Climate change effects on seasonal temperatures may therefore substantially alter future AM fungal community dynamics and ecosystem functioning.

amoA Gene Abundances and Nitrification Potential Rates Suggest that Benthic Ammonia-Oxidizing Bacteria and Not Archaea Dominate N Cycling in the Colne Estuary, United Kingdom

ABSTRACT Nitrification, mediated by ammonia-oxidizing bacteria (AOB) and ammonia-oxidizing archaea (AOA), is important in global nitrogen cycling. In estuaries where gradients of salinity and ammonia concentrations occur, there may be differential selections for ammonia-oxidizer populations. The aim of this study was to examine the activity, abundance, and diversity of AOA and AOB in surface oxic sediments of a highly nutrified estuary that exhibits gradients of salinity and ammonium. AOB and AOA communities were investigated by measuring ammonia monooxygenase (amoA) gene abundance and nitrification potentials both spatially and temporally. Nitrification potentials differed along the estuary and over time, with the greatest nitrification potentials occurring mid-estuary (8.2 μmol N grams dry weight [gdw]−1 day−1 in June, increasing to 37.4 μmol N gdw−1 day−1 in January). At the estuary head, the nitrification potential was 4.3 μmol N gdw−1 day−1 in June, increasing to 11.7 μmol N gdw−1 day−1 in January. At the estuary head and mouth, nitrification potentials fluctuated throughout the year. AOB amoA gene abundances were significantly greater (by 100-fold) than those of AOA both spatially and temporally. Nitrosomonas spp. were detected along the estuary by denaturing gradient gel electrophoresis (DGGE) band sequence analysis. In conclusion, AOB dominated over AOA in the estuarine sediments, with the ratio of AOB/AOA amoA gene abundance increasing from the upper (freshwater) to lower (marine) regions of the Colne estuary. These findings suggest that in this nutrified estuary, AOB (possibly Nitrosomonas spp.) were of major significance in nitrification.

Characterization of geographically distinct bacterial communities associated with coral mucus produced by Acropora spp. and Porites spp.

ABSTRACT Acropora and Porites corals are important reef builders in the Indo-Pacific and Caribbean. Bacteria associated with mucus produced by Porites spp. and Acropora spp. from Caribbean (Punta Maroma, Mexico) and Indo-Pacific (Hoga and Sampela, Indonesia) reefs were determined. Analysis of pyrosequencing libraries showed that bacterial communities from Caribbean corals were significantly more diverse (H′, 3.18 to 4.25) than their Indonesian counterparts (H′, 2.54 to 3.25). Dominant taxa were Gammaproteobacteria, Alphaproteobacteria, Firmicutes, and Cyanobacteria, which varied in relative abundance between coral genera and region. Distinct coral host-specific communities were also found; for example, Clostridiales were dominant on Acropora spp. (at Hoga and the Mexican Caribbean) compared to Porites spp. and seawater. Within the Gammproteobacteria, Halomonas spp. dominated sequence libraries from Porites spp. (49%) and Acropora spp. (5.6%) from the Mexican Caribbean, compared to the corresponding Indonesian coral libraries (<2%). Interestingly, with the exception of Porites spp. from the Mexican Caribbean, there was also a ubiquity of Psychrobacter spp., which dominated Acropora and Porites libraries from Indonesia and Acropora libraries from the Caribbean. In conclusion, there was a dominance of Halomonas spp. (associated with Acropora and Porites [Mexican Caribbean]), Firmicutes (associated with Acropora [Mexican Caribbean] and with Acropora and Porites [Hoga]), and Cyanobacteria (associated with Acropora and Porites [Hoga] and Porites [Sampela]). This is also the first report describing geographically distinct Psychrobacter spp. associated with coral mucus. In addition, the predominance of Clostridiales associated with Acropora spp. provided additional evidence for coral host-specific microorganisms.

Local Adaptation to Soil Hypoxia Determines the Structure of an Arbuscular Mycorrhizal Fungal Community in Roots from Natural CO2 Springs

ABSTRACT The processes responsible for producing and maintaining the diversity of natural arbuscular mycorrhizal (AM) fungal communities remain largely unknown. We used natural CO2 springs (mofettes), which create hypoxic soil environments, to determine whether a long-term, directional, abiotic selection pressure could change AM fungal community structure and drive the selection of particular AM fungal phylotypes. We explored whether those phylotypes that appear exclusively in hypoxic soils are local specialists or widespread generalists able to tolerate a range of soil conditions. AM fungal community composition was characterized by cloning, restriction fragment length polymorphism typing, and the sequencing of small subunit rRNA genes from roots of four plant species growing at high (hypoxic) and low (control) geological CO2 exposure. We found significant levels of AM fungal community turnover (β diversity) between soil types and the numerical dominance of two AM fungal phylotypes in hypoxic soils. Our results strongly suggest that direct environmental selection acting on AM fungi is a major factor regulating AM fungal communities and their phylogeographic patterns. Consequently, some AM fungi are more strongly associated with local variations in the soil environment than with their host plants distribution.

Networking our way to better ecosystem service provision

The ecosystem services (EcoS) concept is being used increasingly to attach values to natural systems and the multiple benefits they provide to human societies. Ecosystem processes or functions only become EcoS if they are shown to have social and/or economic value. This should assure an explicit connection between the natural and social sciences, but EcoS approaches have been criticized for retaining little natural science. Preserving the natural, ecological science context within EcoS research is challenging because the multiple disciplines involved have very different traditions and vocabularies (common-language challenge) and span many organizational levels and temporal and spatial scales (scale challenge) that define the relevant interacting entities (interaction challenge). We propose a network-based approach to transcend these discipline challenges and place the natural science context at the heart of EcoS research.

Fungi in the future: interannual variation and effects of atmospheric change on arbuscular mycorrhizal fungal communities

Understanding the natural dynamics of arbuscular mycorrhizal (AM) fungi and their response to global environmental change is essential for the prediction of future plant growth and ecosystem functions. We investigated the long-term temporal dynamics and effect of elevated atmospheric carbon dioxide (CO2) and ozone (O3) concentrations on AM fungal communities. Molecular methods were used to characterize the AM fungal communities of soybean (Glycine max) grown under elevated and ambient atmospheric concentrations of both CO2 and O3 within a free air concentration enrichment experiment in three growing seasons over 5 yr. Elevated CO2 altered the community composition of AM fungi, increasing the ratio of Glomeraceae to Gigasporaceae. By contrast, no effect of elevated O3 on AM fungal communities was detected. However, the greatest compositional differences detected were between years, suggesting that, at least in the short term, large-scale interannual temporal dynamics are stronger mediators than atmospheric CO2 concentrations of AM fungal communities. We conclude that, although atmospheric change may significantly alter AM fungal communities, this effect may be masked by the influences of natural changes and successional patterns through time. We suggest that changes in carbon availability are important determinants of the community dynamics of AM fungi.

Differences between aerobic and anaerobic degradation of microphytobenthic biofilm-derived organic matter within intertidal sediments

Within intertidal sediments, much of the dissolved organic carbon (DOC) consists of carbohydrate-rich extracellular polymeric substances (EPS) produced by microphytobenthic biofilms. EPS are an important source of carbon and energy for aerobic and anaerobic microorganisms owing to burial of microphytobenthos and downward transport of their exudates. We established slurries of estuarine biofilms to determine the fate of organic carbon and EPS fractions, differing in size and complexity, under oxic and anoxic conditions. DOC and hot-water-extracted organic matter (predominately diatom chrysolaminarin) were utilised rapidly at similar rates in both conditions. Concentrations of insoluble, high-molecular-weight EPS were unchanged in oxic microcosms, but were significantly degraded under anoxic conditions (39% degradation by day 25). Methanogenesis and sulphate reduction were major anaerobic processes in the anoxic slurries, and 16S rRNA gene pyrosequencing revealed that Desulfobacteraceae (relative sequence abundance increased from 1.9% to 12.2%) and Desulfobulbaceae (increased from 1.5% to 4.3%) were the main sulphate reducers, whilst Clostridia and Bacteroidetes were likely responsible for anaerobic hydrolysis and fermentation of EPS. We conclude that a diverse consortium of anaerobic microorganisms (including coexisting sulphate reducers and methanogens) degrade both labile and refractory microphytobenthic-derived carbon and that anaerobic degradation may be the primary fate of more structurally complex components of microphytobenthic EPS.

Nitrate reduction functional genes and nitrate reduction potentials persist in deeper estuarine sediments why

Denitrification and dissimilatory nitrate reduction to ammonium (DNRA) are processes occurring simultaneously under oxygen-limited or anaerobic conditions, where both compete for nitrate and organic carbon. Despite their ecological importance, there has been little investigation of how denitrification and DNRA potentials and related functional genes vary vertically with sediment depth. Nitrate reduction potentials measured in sediment depth profiles along the Colne estuary were in the upper range of nitrate reduction rates reported from other sediments and showed the existence of strong decreasing trends both with increasing depth and along the estuary. Denitrification potential decreased along the estuary, decreasing more rapidly with depth towards the estuary mouth. In contrast, DNRA potential increased along the estuary. Significant decreases in copy numbers of 16S rRNA and nitrate reducing genes were observed along the estuary and from surface to deeper sediments. Both metabolic potentials and functional genes persisted at sediment depths where porewater nitrate was absent. Transport of nitrate by bioturbation, based on macrofauna distributions, could only account for the upper 10 cm depth of sediment. A several fold higher combined freeze-lysable KCl-extractable nitrate pool compared to porewater nitrate was detected. We hypothesised that his could be attributed to intracellular nitrate pools from nitrate accumulating microorganisms like Thioploca or Beggiatoa. However, pyrosequencing analysis did not detect any such organisms, leaving other bacteria, microbenthic algae, or foraminiferans which have also been shown to accumulate nitrate, as possible candidates. The importance and bioavailability of a KCl-extractable nitrate sediment pool remains to be tested. The significant variation in the vertical pattern and abundance of the various nitrate reducing genes phylotypes reasonably suggests differences in their activity throughout the sediment column. This raises interesting questions as to what the alternative metabolic roles for the various nitrate reductases could be, analogous to the alternative metabolic roles found for nitrite reductases.

Belowground DNA-based techniques: untangling the network of plant root interactions

Plant roots are a central driver of ecosystem productivity, as plant investments belowground often comprise more than half of total plant biomass (Jackson et al. 1996). Despite this general observation, almost nothing is known about the distribution of roots in ecosystems; generally because roots of different species are morphologically indistinguishable, restricting species identification. This is in strict contrast to plant identification aboveground, which is straightforward after initial taxonomic training. Although in species poor systems containing roots of two species morphological identification has been possible in a few cases (Genney et al. 2002; Janecek et al. 2004; Mommer et al. 2011), disentangling and identifying roots from species-rich systems is impossible. To overcome problems of species identification, pioneering DNA-based techniques have been applied to plant roots (Jackson et al. 1999; Linder et al. 2000) and are now being used in experimental and observational studies of species-rich plant communities (e.g. Mommer et al. 2010; Kesanakurti et al. 2011; Dumbrell et al. 2011). In this paper, we discuss the current state of molecular techniques for plant species identification and quantification from mixed root samples. We focus on crucial aspects in the methodology regarding primer choice, DNA extraction and PCR inhibition, showing the potential caveats and their solutions. Finally we briefly discuss a few questions in the field of root ecology that will be advanced significantly by the appropriate use of these molecular tools.