Determinants of the Distribution of Nitrogen-cycling Microbial Communities at the Landscape Scale

Overview

Journal ISME J

Publisher Oxford University Press

Specialties Environmental Health
Microbiology

Date 2010 Aug 13

PMID 20703315

Citations 89

Authors

D Bru

A Ramette

N P A Saby

S Dequiedt

L Ranjard

C Jolivet

D Arrouays

L Philippot

Affiliations

Soon will be listed here.

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.

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References

He J, Shen J, Zhang L, Zhu Y, Zheng Y, Xu M . Quantitative analyses of the abundance and composition of ammonia-oxidizing bacteria and ammonia-oxidizing archaea of a Chinese upland red soil under long-term fertilization practices. Environ Microbiol. 2007; 9(9):2364-74. DOI: 10.1111/j.1462-2920.2007.01358.x. View

Cottenie K . Integrating environmental and spatial processes in ecological community dynamics. Ecol Lett. 2011; 8(11):1175-82. DOI: 10.1111/j.1461-0248.2005.00820.x. View

Nunan N, Wu K, Young I, Crawford J, Ritz K . In situ spatial patterns of soil bacterial populations, mapped at multiple scales, in an arable soil. Microb Ecol. 2002; 44(4):296-305. DOI: 10.1007/s00248-002-2021-0. View

Okano Y, Hristova K, Leutenegger C, Jackson L, Ford Denison R, Gebreyesus B . Application of real-time PCR to study effects of ammonium on population size of ammonia-oxidizing bacteria in soil. Appl Environ Microbiol. 2004; 70(2):1008-16. PMC: 348910. DOI: 10.1128/AEM.70.2.1008-1016.2004. View

Bru D, Sarr A, Philippot L . Relative abundances of proteobacterial membrane-bound and periplasmic nitrate reductases in selected environments. Appl Environ Microbiol. 2007; 73(18):5971-4. PMC: 2074903. DOI: 10.1128/AEM.00643-07. View

Nicol G, Leininger S, Schleper C, Prosser J . The influence of soil pH on the diversity, abundance and transcriptional activity of ammonia oxidizing archaea and bacteria. Environ Microbiol. 2008; 10(11):2966-78. DOI: 10.1111/j.1462-2920.2008.01701.x. View

Klappenbach J, Saxman P, Cole J, Schmidt T . rrndb: the Ribosomal RNA Operon Copy Number Database. Nucleic Acids Res. 2000; 29(1):181-4. PMC: 29826. DOI: 10.1093/nar/29.1.181. View

Franklin R, Blum L, McComb A, Mills A . A geostatistical analysis of small-scale spatial variability in bacterial abundance and community structure in salt marsh creek bank sediments. FEMS Microbiol Ecol. 2003; 42(1):71-80. DOI: 10.1111/j.1574-6941.2002.tb00996.x. View

Henry S, Baudoin E, Lopez-Gutierrez J, Martin-Laurent F, Brauman A, Philippot L . Quantification of denitrifying bacteria in soils by nirK gene targeted real-time PCR. J Microbiol Methods. 2004; 59(3):327-35. DOI: 10.1016/j.mimet.2004.07.002. View

10.

Peres-Neto P, Legendre P, Dray S, Borcard D . Variation partitioning of species data matrices: estimation and comparison of fractions. Ecology. 2006; 87(10):2614-25. DOI: 10.1890/0012-9658(2006)87[2614:vposdm]2.0.co;2. View

11.

Ritz K, McNicol J, Nunan N, Grayston S, Millard P, Atkinson D . Spatial structure in soil chemical and microbiological properties in an upland grassland. FEMS Microbiol Ecol. 2009; 49(2):191-205. DOI: 10.1016/j.femsec.2004.03.005. View

12.

Yergeau E, Bezemer T, Hedlund K, Mortimer S, Kowalchuk G, van der Putten W . Influences of space, soil, nematodes and plants on microbial community composition of chalk grassland soils. Environ Microbiol. 2011; 12(8):2096-106. DOI: 10.1111/j.1462-2920.2009.02053.x. View

13.

Ramette A, Tiedje J . Biogeography: an emerging cornerstone for understanding prokaryotic diversity, ecology, and evolution. Microb Ecol. 2006; 53(2):197-207. DOI: 10.1007/s00248-005-5010-2. View

14.

Drenovsky R, Steenwerth K, Jackson L, Scow K . Land use and climatic factors structure regional patterns in soil microbial communities. Glob Ecol Biogeogr. 2014; 19(1):27-39. PMC: 3891896. DOI: 10.1111/j.1466-8238.2009.00486.x. View

15.

Morvan X, Saby N, Arrouays D, Le Bas C, Jones R, Verheijen F . Soil monitoring in Europe: a review of existing systems and requirements for harmonisation. Sci Total Environ. 2007; 391(1):1-12. DOI: 10.1016/j.scitotenv.2007.10.046. View

16.

Leininger S, Urich T, Schloter M, Schwark L, Qi J, Nicol G . Archaea predominate among ammonia-oxidizing prokaryotes in soils. Nature. 2006; 442(7104):806-9. DOI: 10.1038/nature04983. View

17.

Hallin S, Jones C, Schloter M, Philippot L . Relationship between N-cycling communities and ecosystem functioning in a 50-year-old fertilization experiment. ISME J. 2009; 3(5):597-605. DOI: 10.1038/ismej.2008.128. View

18.

Fierer N, Jackson R . The diversity and biogeography of soil bacterial communities. Proc Natl Acad Sci U S A. 2006; 103(3):626-31. PMC: 1334650. DOI: 10.1073/pnas.0507535103. View

19.

Martin-Laurent F, Philippot L, Hallet S, Chaussod R, Germon J, Soulas G . DNA extraction from soils: old bias for new microbial diversity analysis methods. Appl Environ Microbiol. 2001; 67(5):2354-9. PMC: 92877. DOI: 10.1128/AEM.67.5.2354-2359.2001. View

20.

Hartman W, Richardson C, Vilgalys R, Bruland G . Environmental and anthropogenic controls over bacterial communities in wetland soils. Proc Natl Acad Sci U S A. 2008; 105(46):17842-7. PMC: 2584698. DOI: 10.1073/pnas.0808254105. View