Changes in community composition of ammonia-oxidizing betaproteobacteria from stands of Black mangrove (Avicennia germinans) in response to ammonia enrichment and more oxic conditions

Hendrikus J Laanbroek,Rosalinde M Keijzer,Jos T A Verhoeven,Dennis F Whigham

doi:10.3389/fmicb.2013.00343

Abstract

In flooded and non-flooded impounded forests of Black mangrove (Avicennia germinans), the community structure of the ammonia-oxidizing betaproteobacteria (β-AOB) differed among distinct mangrove vegetation cover types and hydrological regimes. This had been explained by a differential response of lineages of β-AOB to the prevailing soil conditions that included increased levels of moisture and ammonium. To test this hypothesis, slurries of soils collected from a flooded and a non-flooded impoundment were subjected to enhanced levels of ammonium in the absence and presence of additional shaking. After a period of 6 days, the community composition of the β-AOB based on the 16S rRNA gene was determined and compared with the original community structures. Regardless of the incubation conditions and the origin of the samples, sequences belonging to the Nitrosomonas aestuarii lineage became increasingly dominant, whereas the number of sequences of the lineages of Nitrosospira (i.e., Cluster 1) and Nitrosomonas sp. Nm143 declined. Changes in community structure were related to changes in community sizes determined by quantitative PCR based on the amoA gene. The amoA gene copy numbers of β-AOB were compared to those of the ammonia-oxidizing archaea (AOA). Gene copy numbers of the bacteria increased irrespective of incubation conditions, but the numbers of archaea declined in the continuously shaken cultures. This observation is discussed in relation to the distribution of the β-AOB lineages in the impounded Black mangrove forests.

Highlights

Aerobic ammonia-oxidizing archaea and bacteria play an important role in the global nitrogen cycle by converting ammonia to nitrite (Kowalchuk and Stephen, 2001; Schleper and Nicol, 2010)
Studies applying the phylogenetic 16S rRNA gene and the amoA gene that codes for the α-subunit of the enzyme ammonia monooxygenase in aerobic ammonia-oxidizing archaea and bacteria showed that the ammonia-oxidizing thaumarchaea and betaproteobacteria (β-AOB) are widely distributed (Kowalchuk and Stephen, 2001; Schleper and Nicol, 2010) and occur in many habitats, including soils of mangrove forests (e.g., Wickramasinghe et al, 2009.) Mangroves are tree-dominated intertidal wetlands along tropical and subtropical coastlines with a specialized flora adapted to waterlogged and saline conditions
In a previous study (Laanbroek et al, 2012) we investigated the effects of vegetation cover type and summer flooding on the process of ammonia oxidation in soils collected from mangrove stands that were dominated by Black mangrove (Avicennia germinans) of differing statures that occurred in impoundments with dissimilar hydrologic regimes

Summary

Introduction

Aerobic ammonia-oxidizing archaea and bacteria play an important role in the global nitrogen cycle by converting ammonia to nitrite (Kowalchuk and Stephen, 2001; Schleper and Nicol, 2010). Studies applying the phylogenetic 16S rRNA gene and the amoA gene that codes for the α-subunit of the enzyme ammonia monooxygenase in aerobic ammonia-oxidizing archaea and bacteria showed that the ammonia-oxidizing thaumarchaea and betaproteobacteria (β-AOB) are widely distributed (Kowalchuk and Stephen, 2001; Schleper and Nicol, 2010) and occur in many habitats, including soils of mangrove forests (e.g., Wickramasinghe et al, 2009.) Mangroves are tree-dominated intertidal wetlands along tropical and subtropical coastlines with a specialized flora adapted to waterlogged and saline conditions. In a previous study (Laanbroek et al, 2012) we investigated the effects of vegetation cover type and summer flooding on the process of ammonia oxidation in soils collected from mangrove stands that were dominated by Black mangrove (Avicennia germinans) of differing statures that occurred in impoundments with dissimilar hydrologic regimes. Since higher moisture levels are generally associated with more reduced conditions in the soils, it can be argued that members of the Nitrosomonas Nm143 lineage are better adapted www.frontiersin.org

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