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

Kateryna Zhalnina,Penny R Hirsch,Jennifer C Drew,Patricia D De Quadros,Samira H Daroub,Adriana Giongo,Luis A Sayavedra-Soto,Flavio A O Camargo,Kelsey A Gano,Dan J Arp,Steve P Mcgrath,Ian M Clark,Austin Davis-Richardson,Jennie R Fagen,Eric W Triplett,Christopher T Brown

doi:10.3389/fmicb.2013.00104

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.

Highlights

The transformation of soil to agricultural use causes significant changes in its chemical, physical, and biological features, including changes in the microbial community composition (Kibblewhite et al, 2008)
It was found that nitrogen (N) deposition increases the abundance of certain microbial phyla, such as Actinobacteria, Proteobacteria, Bacteroidetes, and Firmicutes, but it decreases the abundance of other bacterial phyla, such as Acidobacteria and Verrucomicrobia (Ramirez et al, 2010, 2012; Fierer et al, 2012)
SEQUENCE ANALYSIS OF 16S rRNA GENES AND MICROBIAL COMMUNITY AT AGRICULTURAL AND NON-AGRICULTURAL SITES The total number of barcoded reads obtained from sequencing ranged between 1.3 and 11.4 million reads with an average length of 158 bp (Table 1). 94.3%, 95.5%, and 91.1% sequences were classified as Bacteria; 3%, 1.3%, and 3.7% sequences as Archaea at Broadbalk Rothamsted Research (BRR), Kellogg Biological Station (KBS), and Everglades Agricultural Area (EAA), respectively

Summary

Introduction

The transformation of soil to agricultural use causes significant changes in its chemical, physical, and biological features, including changes in the microbial community composition (Kibblewhite et al, 2008). A number of studies have examined the impact of agriculture on microbial community structure. Other studies have focused on the changes of specific microbial taxa involved in nutrient cycling in soil, such as diazotrophs (Meng et al, 2012), nitrifiers (Chu et al, 2008), and denitrifiers (Clark et al, 2012) under specific agricultural management. All studies of the agricultural impact on the microbial community are limited either to the phylum level, which represents a large and diverse set of functional microbial groups, or to the specific physiological group. We hypothesize that there are common microbial taxa strongly associated with agricultural land use, and these taxa can be used as indicators www.frontiersin.org

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