Changes in the community structure of ammonia‐oxidizing bacteria during secondary succession of calcareous grasslands

Abstract

The community structure of beta-subclass Proteobacteria ammonia-oxidizing bacteria was determined in semi-natural chalk grassland soils at different stages of secondary succession. Both culture-mediated (most probable number; MPN) and direct nucleic acid-based approaches targeting genes encoding 16S rRNA and the AmoA subunit of ammonia monooxygenase were used. Similar shifts were detected in the composition of the ammonia oxidizer communities by both culture-dependent and independent approaches. A predominance of Nitrosospira sequence cluster 3 in early successional fields was replaced by Nitrosospira sequence cluster 4 in late successional fields. The rate of this shift differed between the two areas examined. This shift occurred in a background of relative stability in the dominant bacterial populations in the soil, as determined by domain-level polymerase chain reaction-denaturing gradient gel electrophoresis (PCR-DGGE). Molecular analysis of enrichment cultures obtained using different ammonia concentrations revealed biases towards Nitrosospira sequence cluster 3 or Nitrosospira sequence cluster 4 under high- or low-ammonia conditions respectively. High-ammonia MPNs suggested a decease in ammonia oxidizer numbers with succession, but low-ammonia MPNs and competitive PCR targeting amoA failed to support such a trend. Ammonia turnover rate, not specific changes in plant diversity and species composition, is implicated as the major determinant of ammonia oxidizer community structure in successional chalk grassland soils.

The Biogeography of Ammonia-Oxidizing Bacterial Communities in Soil

“…However, while Nitrosopira cluster 2 was relatively abundant in three forest soil libraries (BF1, BZ2, BZ3) with reasonably low pHs (4.05-5.36), there was no overall correlation between the relative abundances of cluster 2 in the libraries and soil pH (ρ=0.15, P=0.3) suggesting that cluster 2 AOB do not necessarily have higher relative abundances in acidic soils. Likewise, results from previous studies [14][15][16]20] have contributed to the hypothesis that representatives of Nitrosospira cluster 3 are likely to be relatively more abundant in soils with higher levels of N availability. If we examine the proportional abundances of Nitrosospira cluster 3, we see no correlations with our measured indices of N availability (N mineralization rates and extractable NH 4 + or the sum of NH 4 + plus NO 3 − concentrations, P>0.4 in all cases).…”

“…We do know that distinct soils often harbor distinct AOB communities. A number of environmental factors, including vegetation type [9][10][11], soil nutrient levels [12][13][14][15][16], soil microclimate [13,17,18], and management practices [19][20][21], have been found to have an important influence on the spatial variability exhibited by AOB communities. However, because most studies have compared AOB communities across a rather limited number of samples, with one notable exception being the study by Avrahami and Conrad [18], it has been difficult to ascertain which soil biotic and abiotic characteristics are related to AOB community composition across larger spatial scales.…”

Nitrogen and phosphorus enrichment alter the composition of ammonia-oxidizing bacteria in salt marsh sediments

“…Studies from a variety of habitats document that AOB communities vary over space (Kowalchuk and Stephen, 2001) and that this variation is correlated with a variety of factors, including salinity (Stehr et al, 1995;Sahan and Muyzer, 2008), temperature (Avrahami and Conrad, 2005;Fierer et al, 2009), nutrients (Webster et al, 2002;Mosier and Francis, 2008), plant composition (Briones et al, 2002;Mintie et al, 2003;Dollhopf et al, 2005), soil moisture (Hastings et al, 2000) and pH (Kowalchuk et al, 2000;Nicol et al, 2008). Field experiments confirm that pH (Stephen et al, 1998;Backman et al, 2003) and nitrogen availability (Phillips et al, 2000;Webster et al, 2002) can directly influence AOB composition and/or abundance.…”

“…Depending on the environmental conditions, nitrification can positively or negatively affect nitrogen retention in ecosystems (Kowalchuk et al, 2000;Templer et al, 2008;von Schiller et al, 2009). At the same time, the composition of nitrifying microorganisms can influence nitrification rates (Bottomley et al, 2004;Balser and Firestone, 2005;Bernhard et al, 2007).…”

Studies on the restoration succession of PFU microbial communities in a pilot-scale microcosm

“…Many works have been reported to study the structural and functional variables of aquatic communities in relation to the ecological succession (Kowalchuk et al, 2000;Kelly and Chistoserdov, 2001;Merila et al, 2002;Noll et al, 2005;Michail et al, 2005). Since the last decade of last century, nature management has embodied a lot of projects to restore damaged ecosystems (Hemerik and Brussaard, 2002;Clewell and Aronson, 2006).…”