Differential responses of ammonia-oxidizing archaea and bacteria to long-term fertilization in a New England salt marsh

Xuefeng Peng,Courtney Dwyer,Anne Kearney,Ivan Valiela,Erica Hildebrand,Alex Waciega,Erik Yando,Anne E Bernhard

doi:10.3389/fmicb.2012.00445

Abstract

Since the discovery of ammonia-oxidizing archaea (AOA), new questions have arisen about population and community dynamics and potential interactions between AOA and ammonia-oxidizing bacteria (AOB). We investigated the effects of long-term fertilization on AOA and AOB in the Great Sippewissett Marsh, Falmouth, MA, USA to address some of these questions. Sediment samples were collected from low and high marsh habitats in July 2009 from replicate plots that received low (LF), high (HF), and extra high (XF) levels of a mixed NPK fertilizer biweekly during the growing season since 1974. Additional untreated plots were included as controls (C). Terminal restriction fragment length polymorphism analysis of the amoA genes revealed distinct shifts in AOB communities related to fertilization treatment, but the response patterns of AOA were less consistent. Four AOB operational taxonomic units (OTUs) predictably and significantly responded to fertilization, but only one AOA OTU showed a significant pattern. Betaproteobacterial amoA gene sequences within the Nitrosospira-like cluster dominated at C and LF sites, while sequences related to Nitrosomonas spp. dominated at HF and XF sites. We identified some clusters of AOA sequences recovered primarily from high fertilization regimes, but other clusters consisted of sequences recovered from all fertilization treatments, suggesting greater physiological diversity. Surprisingly, fertilization appeared to have little impact on abundance of AOA or AOB. In summary, our data reveal striking patterns for AOA and AOB in response to long-term fertilization, and also suggest a missing link between community composition and abundance and nitrogen processing in the marsh.

Highlights

Oxidation of ammonia to nitrite is a critical process in nitrogen cycling and is carried out by a suite of distinct microorganisms within the bacterial and archaeal domains
SHIFTS IN ammonia-oxidizing bacteria (AOB) COMMUNITY COMPOSITION Terminal restriction fragment length polymorphism analysis of betaproteobacterial amoA genes revealed a total of 12 terminal restriction fragments (TRFs) and an average of 8.3 TRFs per sample
AOB COMMUNITY COMPOSITION AND RESPONSE TO FERTILIZATION We found significant shifts in AOB communities that corresponded to fertilization, which is in agreement with several previous studies of AOB in fertilized soils and sediments (Chu et al, 2007; Shen et al, 2011; Wu et al, 2011)

Summary

Introduction

Oxidation of ammonia to nitrite is a critical process in nitrogen cycling and is carried out by a suite of distinct microorganisms within the bacterial and archaeal domains. Researchers have made great progress in describing the diversity and distribution of ammonia-oxidizing bacteria (AOB) in estuaries (see review by Bernhard and Bollmann, 2010) and to a lesser extent in salt marshes (Dollhopf et al, 2005; Moin et al, 2009). Most studies have reported salinity to be a major factor regulating the distribution and diversity of AOB in these coastal systems (Francis et al, 2003; Bernhard et al, 2005; Ward et al, 2007). With the recent discovery of ammonia-oxidizing archaea (AOA; Könneke et al, 2005; Treusch et al, 2005) and their apparent wide distribution in many habitats, the relative importance of AOB to nitrification and their potential interactions with AOA have been brought into question

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