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Determinants of the distribution of nitrogen-cycling microbial communities at the landscape scale.

ABSTRACT: Little information is available regarding the landscape-scale distribution of microbial communities and its environmental determinants. However, a landscape perspective is needed to understand the relative importance of local and regional factors and land management for the microbial communities and the ecosystem services they provide. In the most comprehensive analysis of spatial patterns of microbial communities to date, we investigated the distribution of functional microbial communities involved in N-cycling and of the total bacterial and crenarchaeal communities over 107 sites in Burgundy, a 31,500 km(2) region of France, using a 16 × 16 km(2) sampling grid. At each sampling site, the abundance of total bacteria, crenarchaea, nitrate reducers, denitrifiers- and ammonia oxidizers were estimated by quantitative PCR and 42 soil physico-chemical properties were measured. The relative contributions of land use, spatial distance, climatic conditions, time, and soil physico-chemical properties to the spatial distribution of the different communities were analyzed by canonical variation partitioning. Our results indicate that 43-85% of the spatial variation in community abundances could be explained by the measured environmental parameters, with soil chemical properties (mostly pH) being the main driver. We found spatial autocorrelation up to 739 km and used geostatistical modelling to generate predictive maps of the distribution of microbial communities at the landscape scale. The present study highlights the potential of a spatially explicit approach for microbial ecology to identify the overarching factors driving the spatial heterogeneity of microbial communities even at the landscape scale.

SUBMITTER: Bru D

PROVIDER: S-EPMC3105713 | biostudies-literature | 2011 Mar

REPOSITORIES: biostudies-literature

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Determinants of the distribution of nitrogen-cycling microbial communities at the landscape scale.

Bru D D Ramette A A Saby N P A NP Dequiedt S S Ranjard L L Jolivet C C Arrouays D D Philippot L L

The ISME journal 20100812 3

Little information is available regarding the landscape-scale distribution of microbial communities and its environmental determinants. However, a landscape perspective is needed to understand the relative importance of local and regional factors and land management for the microbial communities and the ecosystem services they provide. In the most comprehensive analysis of spatial patterns of microbial communities to date, we investigated the distribution of functional microbial communities invo ...[more]

PMID: 20703315

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Project description:Microorganisms drive much of the marine nitrogen (N) cycle, which jointly controls the primary production in the global ocean. However, our understanding of the microbial communities driving the global ocean N cycle remains fragmented. Focusing on "who is doing what, where, and how?", this study draws a clear picture describing the global biogeography of marine N-cycling microbial communities by utilizing the Tara Oceans shotgun metagenomes. The marine N-cycling communities are highly variable taxonomically but relatively even at the functional trait level, showing clear functional redundancy properties. The functional traits and taxonomic groups are shaped by the same set of geo-environmental factors, among which, depth is the major factor impacting marine N-cycling communities, differentiating mesopelagic from epipelagic communities. Latitudinal diversity gradients and distance-decay relationships are observed for taxonomic groups, but rarely or weakly for functional traits. The composition of functional traits is strongly deterministic as revealed by null model analysis, while a higher degree of stochasticity is observed for taxonomic composition. Integrating multiple lines of evidence, in addition to drawing a biogeographic picture of marine N-cycling communities, this study also demonstrated an essential microbial ecological theory-determinism governs the assembly of microbial communities performing essential biogeochemical processes; the environment selects functional traits rather than taxonomic groups; functional redundancy underlies stochastic taxonomic community assembly. IMPORTANCE A critical question in microbial ecology is how the complex microbial communities are formed in natural ecosystems with the existence of thousands different species, thereby performing essential ecosystem functions and maintaining ecosystem stability. Previous studies disentangling the community assembly mechanisms mainly focus on microbial taxa, ignoring the functional traits they carry. By anchoring microbial functional traits and their carrying taxonomic groups involved in nitrogen cycling processes, this study demonstrated an important mechanism associated with the complex microbial community assembly. Evidence shows that the environment selects functional traits rather than taxonomic groups, and functional redundancy underlies stochastic taxonomic community assembly. This study is expected to provide valuable mechanistic insights into the complex microbial community assembly in both natural and artificial ecosystems.

Project description:IntroductionThe expanded granular sludge bed (EGSB) is a major form of anaerobic digestion system during wastewater treatment. Yet, the dynamics of microbial and viral communities and members functioning in nitrogen cycling along with monthly changing physicochemical properties have not been well elucidated.MethodsHere, by collecting the anaerobic activated sludge samples from a continuously operating industrial-scale EGSB reactor, we conducted 16S rRNA gene amplicon sequencing and metagenome sequencing to reveal the microbial community structure and variation with the ever-changing physicochemical properties along within a year.ResultsWe observed a clear monthly variation of microbial community structures, while COD, the ratio of volatile suspended solids (VSS) to total suspended solids (TSS) (VSS/TSS ratio), and temperature were predominant factors in shaping community dissimilarities examined by generalized boosted regression modeling (GBM) analysis. Meanwhile, a significant correlation was found between the changing physicochemical properties and microbial communities (p <0.05). The alpha diversity (Chao1 and Shannon) was significantly higher (p <0.05) in both winter (December, January, and February) and autumn (September, October, and November) with higher organic loading rate (OLR), higher VSS/TSS ratio, and lower temperature, resulting higher biogas production and nutrition removal efficiency. Further, 18 key genes covering nitrate reduction, denitrification, nitrification, and nitrogen fixation pathways were discovered, the total abundance of which was significantly associated with the changing environmental factors (p <0.05). Among these pathways, the dissimilatory nitrate reduction to ammonia (DNRA) and denitrification had the higher abundance contributed by the top highly abundant genes narGH, nrfABCDH, and hcp. The COD, OLR, and temperature were primary factors in affecting DNRA and denitrification by GBM evaluation. Moreover, by metagenome binning, we found the DNRA populations mainly belonged to Proteobacteria, Planctomycetota, and Nitrospirae, while the denitrifying bacteria with complete denitrification performance were all Proteobacteria. Besides, we detected 3,360 non-redundant viral sequences with great novelty, in which Siphoviridae, Podoviridae, and Myoviridae were dominant viral families. Interestingly, viral communities likewise depicted clear monthly variation and had significant associations with the recovered populations (p <0.05).DiscussionOur work highlights the monthly variation of microbial and viral communities during the continuous operation of EGSB affected by the predominant changing COD, OLR, and temperature, while DNRA and denitrification pathways dominated in this anaerobic system. The results also provide a theoretical basis for the optimization of the engineered system.

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Determinants of the distribution of nitrogen-cycling microbial communities at the landscape scale.

Publications

Determinants of the distribution of nitrogen-cycling microbial communities at the landscape scale.

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