Ca. Nitrososphaera and Bradyrhizobium are inversely correlated and related to agricultural practices in long-term field experiments

Abstract

Agricultural land management, such as fertilization, liming, and tillage affects soil properties, including pH, organic matter content, nitrification rates, and the microbial community. Three different study sites were used to identify microorganisms that correlate with agricultural land use and to determine which factors regulate the relative abundance of the microbial signatures of the agricultural land-use. The three sites included in this study are the Broadbalk Experiment at Rothamsted Research, UK, the Everglades Agricultural Area, Florida, USA, and the Kellogg Biological Station, Michigan, USA. The effects of agricultural management on the abundance and diversity of bacteria and archaea were determined using high throughput, barcoded 16S rRNA sequencing. In addition, the relative abundance of these organisms was correlated with soil features. Two groups of microorganisms involved in nitrogen cycle were highly correlated with land use at all three sites. The ammonia oxidizing-archaea, dominated by Ca. Nitrososphaera, were positively correlated with agriculture while a ubiquitous group of soil bacteria closely related to the diazotrophic symbiont, Bradyrhizobium, was negatively correlated with agricultural management. Analysis of successional plots showed that the abundance of ammonia oxidizing-archaea declined and the abundance of bradyrhizobia increased with time away from agriculture. This observation suggests that the effect of agriculture on the relative abundance of these genera is reversible. Soil pH and NH3 concentrations were positively correlated with archaeal abundance but negatively correlated with the abundance of Bradyrhizobium. The high correlations of Ca. Nitrososphaera and Bradyrhizobium abundances with agricultural management at three long-term experiments with different edaphoclimatic conditions allowed us to suggest these two genera as signature microorganisms for agricultural land use.

Soil resilience and recovery: rapid community responses to management changes

“…Their key role in the N cycle is producing nitrite for the second step in nitrification: the abundance estimated from their specific amoA genes g −1 dry soil in permanent arable plots was significantly greater than in either bare fallow or grassland. This is presumably due to a lack of substrate (no fertilizer ammonia added, in contrast to the arable treatments) with an additional effect due to the selective disadvantage of the archaea in the undisturbed grassland soil (Zhalnina et al 2013). Conversion of arable plots to bare fallow or grassland, where no fertilizer was applied, resulted in a decrease in ammonia-oxidizing bacteria; they increased significantly when bare fallow or grassland plots were converted to arable.…”

“…Increased N supply will favour certain groups of microorganisms including nitrifiers that oxidize ammonia and nitrite as an energy source, and denitrifiers that can use nitrate as an electron acceptor when conditions become anaerobic. Perennial untilled and arable, fertilized, tilled treatments appear to favour distinct groups of microorganisms; different from communities in soil receiving no plant or fertilizer inputs (Zhalnina et al 2013). In addition to these overarching effects, there are temporal fluctuations in soil microbial community structure within replicate plots, albeit less marked than between treatments (Lauber et al 2013).…”

“…DNA samples and PCR results failing to meet our quality criteria were discarded: a full description of the primers, PCR conditions and quality controls has been described previously (Cardenas et al 2013;Clark et al 2012) and is provided in the Supplementary Information. We did not quantify archaeal 16S rRNA genes: previous results indicated that they were 100-times less frequent than bacteria in our soils and the vast majority were ammonia oxidizers, so would be enumerated by the primers for archaeal amoA (Zhalnina et al 2013). For community analysis using amplicon sequencing, one pooled DNA sample from each plot was used, providing 3 replicates per treatment.…”

“…Many studies show differences in communities from soils with contrasting treatments Garbeva et al 2008;Geisseler and Scow 2014;de Quadros et al 2012;Zhalnina et al 2013). In non-agricultural systems there is evidence for the development of distinct bacterial communities selected over centuries (Cutler et al 2014;Jangid et al 2011) and fungal communities over decades (Hogberg et al 2014) with soil pH a major factor in microbial community structure at continental, landscape and field scale (Fierer and Jackson 2006;Griffiths et al 2011;Zhalnina et al 2015).…”

“…In addition to these overarching effects, there are temporal fluctuations in soil microbial community structure within replicate plots, albeit less marked than between treatments (Lauber et al 2013). Although comparison of long-term treatments provides evidence that soil management influences soil biota (Hirsch et al 2009;Zhalnina et al 2013Zhalnina et al , 2015, there is scant information on the responses during the early years following change.…”