Meta-analysis reveals ammonia-oxidizing bacteria respond more strongly to nitrogen addition than ammonia-oxidizing archaea

Shifts in microbial communities driven by anthropogenic nitrogen (N) addition have broad-scale ecological consequences. However, responses of microbial groups to exogenous N supply vary considerably across studies, hindering efforts to predict community changes. We used meta-analytical techniques to explore how amoA gene abundances of ammonia-oxidizing archaea (AOA) and bacteria (AOB) respond to N addition, and found that N addition increased AOA and AOB abundances by an average of 27% and 326%, respectively. Responses of AOB varied by study type, ecosystem, fertilizer type, and soil pH, and were strongest in unmanaged wildland soils and soils fertilized with inorganic N sources. Increases in nitrification potential with N addition significantly correlated with only AOB. Our analyses suggest that elevated N supply enhances soil nitrification potential by increasing AOB populations, and that this effect may be most pronounced in unmanaged wildland soils

Long-term impacts of disturbance on nitrogen-cycling bacteria in a New England salt marsh

Recent studies on the impacts of disturbance on microbial communities indicate communities show differential responses to disturbance, yet our understanding of how different microbial communities may respond to and recover from disturbance is still rudimentary. We investigated impacts of tidal restriction followed by tidal restoration on abundance and diversity of denitrifying bacteria, ammonia-oxidizing bacteria (AOB), and ammonia-oxidizing archaea (AOA) in New England salt marshes by analyzing nirS and bacterial and archaeal amoA genes, respectively. TRFLP analysis of nirS and betaproteobacterial amoA genes revealed significant differences between restored and undisturbed marshes, with the greatest differences detected in deeper sediments. Additionally, community patterns indicated a potential recovery trajectory for denitrifiers. Analysis of archaeal amoA genes, however, revealed no differences in community composition between restored and undisturbed marshes, but we detected significantly higher gene abundance in deeper sediment at restored sites. Abundances of nirS and betaproteobacterial amoA genes were also significantly greater in deeper sediments at restored sites. Porewater ammonium was significantly higher at depth in restored sediments compared to undisturbed sediments, suggesting a possible mechanism driving some of the community differences. Our results suggest that impacts of disturbance on denitrifying and ammonia-oxidizing communities remain nearly 30 years after restoration, potentially impacting nitrogen-cycling processes in the marsh. We also present data suggesting that sampling deeper in sediments may be critical for detecting disturbance effects in coastal sediments

The distribution of ammonia-oxidizing betaproteobacteria in stands of Black mangroves (Avicennia germinans)

The distribution of species of aerobic chemolitho-autotrophic microorganisms such as ammonia-oxidizing bacteria are governed by pH, salinity, and temperature as well as the availability of oxygen, ammonium, carbon dioxide, and other inorganic elements required for growth. Impounded mangrove forests in the Indian River Lagoon, a coastal estuary on the east coast of Florida, are dominated by mangroves, especially stands of Black mangrove (Avicennia germinans) that differ in the size and density of individual plants. In March 2009, the management of one impoundment was changed to a regime of pumping estuarine water into the impoundment at critical times of the year to eliminate breeding sites for noxious insects. We collected soil samples in three different Black mangrove habitats before and after the change in management to determine the impacts of the altered hydrologic regimes on the distribution of 16s rRNA genes belonging to ammonia-oxidizing betaproteobacteria (β-AOB). We also sampled soils in an adjacent impoundment in which there had not been any hydrologic alteration. At the level of 97% mutual similarity in the 16s rRNA gene, 13 different operational taxonomic units were identified; the majority related to the lineages of Nitrosomonas marina (45% of the total clones), Nitrosomonas sp. Nm143 (23%), and Nitrosospira cluster 1 (19%). Long-term summer flooding of the impoundment in 2009, after initiation of the pumping regime, reduced the percentage of N. marina by half between 2008 and 2010 in favor of the two other major lineages and the potential ammonia-oxidizing activity decreased by an average of 73%. Higher interstitial salinities, probably due to a prolonged winter drought, had a significant effect on the composition of the β-AOB in March 2009 compared to March 2008: Nitrosomonas sp. Nm143 was replaced by Nitrosospira cluster 1 as the second most important lineage. There were small, but significant differences in the bacterial communities between the flooded and non-flooded impoundments. There were also differences in the community composition of the bacteria in the three Black mangrove habitats. N. marina was most dominant in all three habitats, but was partly replaced by Nitrosospira cluster 1 in sites dominated by sparsely distributed trees and by Nitrosomonas sp. Nm143 in sites characterized by taller, more densely distributed Black mangrove trees.

The ecological dichotomy of ammonia-oxidizing archaea and bacteria in the hyper-arid soils of the Antarctic Dry Valleys

The McMurdo Dry Valleys of Antarctica are considered to be one of the most physically and chemically extreme terrestrial environments on the Earth. However, little is known about the organisms involved in nitrogen transformations in these environments. In this study, we investigated the diversity and abundance of ammonia-oxidizing archaea (AOA) and bacteria (AOB) in four McMurdo Dry Valleys with highly variable soil geochemical properties and climatic conditions: Miers Valley, Upper Wright Valley, Beacon Valley and Battleship Promontory. The bacterial communities of these four Dry Valleys have been examined previously, and the results suggested that the extremely localized bacterial diversities are likely driven by the disparate physicochemical conditions associated with these locations. Here we showed that AOB and AOA amoA gene diversity was generally low; only four AOA and three AOB operational taxonomic units (OTUs) were identified from a total of 420 AOA and AOB amoA clones. Quantitative PCR analysis of amoA genes revealed clear differences in the relative abundances of AOA and AOB amoA genes among samples from the four dry valleys. Although AOB amoA gene dominated the ammonia-oxidizing community in soils from Miers Valley and Battleship Promontory, AOA amoA gene were more abundant in samples from Upper Wright and Beacon Valleys, where the environmental conditions are considerably harsher (e.g., extremely low soil C/N ratios and much higher soil electrical conductivity). Correlations between environmental variables and amoA genes copy numbers, as examined by redundancy analysis (RDA), revealed that higher AOA/AOB ratios were closely related to soils with high salts and Cu contents and low pH. Our findings hint at a dichotomized distribution of AOA and AOB within the Dry Valleys, potentially driven by environmental constraints

Estuarine Nitrifiers: New Players, Patterns and Processes

Ever since the first descriptions of ammonia-oxidizing Bacteria by Winogradsky in the late 1800s, the metabolic capability of aerobic ammonia oxidation has been restricted to a phylogenetically narrow group of bacteria. However, the recent discovery of ammonia-oxidizing Archaea has forced microbiologists and ecologists to re-evaluate long-held paradigms and the role of niche partitioning between bacterial and archaeal ammonia oxidizers. Much of the current research has been conducted in open ocean or terrestrial systems, where community patterns of archaeal and bacterial ammonia oxidizers are highly congruent. Studies of archaeal and bacterial ammonia oxidizers in estuarine systems, however, present a very different picture, with highly variable patterns of archaeal and bacterial ammonia oxidizer abundances. Although salinity is often identified as an important factor regulating abundance, distribution, and diversity of both archaeal and bacterial ammonia oxidizers, the data suggest that the variability in the observed patterns is likely not due to a simple salinity effect. Here we review current knowledge of ammonia oxidizers in estuaries and propose that because of their steep physico-chemical gradients, estuaries may serve as important natural laboratories in which to investigate the relationships between archaeal and bacterial ammonia oxidizers

A positive relationship between the abundance of ammonia oxidizing archaea and natural abundance δ15N of ecosystems

We present a significant relationship between the natural abundance isotopic composition of ecosystem pools and the abundance of a microbial gene. Natural abundance 15N of soils and soil DNA were analysed and compared with archaeal ammonia oxidizer abundance along an elevation gradient in northern Arizona and along a substrate age gradient in Hawai'i. There was a significant positive correlation between the abundance of archaeal amoA genes and natural abundance δ15N of total soil or DNA suggesting that ammonia oxidizing archaea play an important role in ecosystem N release. © 2013 Elsevier Ltd

Distribution and Diversity of Archaeal and Bacterial Ammonia Oxidizers in Salt Marsh Sediments

Diversity and abundance of ammonia-oxidizing Betaproteobacteria (β-AOB) and archaea (AOA) were investigated in a New England salt marsh at sites dominated by short or tall Spartina alterniflora (SAS and SAT sites, respectively) or Spartina patens (SP site). AOA amoA gene richness was higher than β-AOB amoA richness at SAT and SP, but AOA and β-AOB richness were similar at SAS. β-AOB amoA clone libraries were composed exclusively of Nitrosospira-like amoA genes. AOA amoA genes at SAT and SP were equally distributed between the water column/sediment and soil/sediment clades, while AOA amoA sequences at SAS were primarily affiliated with the water column/sediment clade. At all three site types, AOA were always more abundant than β-AOB based on quantitative PCR of amoA genes. At some sites, we detected 109 AOA amoA gene copies g of sediment−1. Ratios of AOA to β-AOB varied over 2 orders of magnitude among sites and sampling dates. Nevertheless, abundances of AOA and β-AOB amoA genes were highly correlated. Abundance of 16S rRNA genes affiliated with Nitrosopumilus maritimus, Crenarchaeota group I.1b, and pSL12 were positively correlated with AOA amoA abundance, but ratios of amoA to 16S rRNA genes varied among sites. We also observed a significant effect of pH on AOA abundance and a significant salinity effect on both AOA and β-ΑΟΒ abundance. Our results expand the distribution of AOA to salt marshes, and the high numbers of AOA at some sites suggest that salt marsh sediments serve as an important habitat for AOA

Expansion of Thaumarchaeota habitat range is correlated with horizontal transfer of ATPase operons.

Thaumarchaeota are responsible for a significant fraction of ammonia oxidation in the oceans and in soils that range from alkaline to acidic. However, the adaptive mechanisms underpinning their habitat expansion remain poorly understood. Here we show that expansion into acidic soils and the high pressures of the hadopelagic zone of the oceans is tightly linked to the acquisition of a variant of the energy-yielding ATPases via horizontal transfer. Whereas the ATPase genealogy of neutrophilic Thaumarchaeota is congruent with their organismal genealogy inferred from concatenated conserved proteins, a common clade of V-type ATPases unites phylogenetically distinct clades of acidophilic/acid-tolerant and piezophilic/piezotolerant species. A presumptive function of pumping cytoplasmic protons at low pH is consistent with the experimentally observed increased expression of the V-ATPase in an acid-tolerant thaumarchaeote at low pH. Consistently, heterologous expression of the thaumarchaeotal V-ATPase significantly increased the growth rate of E. coli at low pH. Its adaptive significance to growth in ocean trenches may relate to pressure-related changes in membrane structure in which this complex molecular machine must function. Together, our findings reveal that the habitat expansion of Thaumarchaeota is tightly correlated with extensive horizontal transfer of atp operons

Population Dynamics and Community Composition of Ammonia Oxidizers in Salt Marshes after the Deepwater Horizon Oil Spill

The recent oil spill in the Gulf of Mexico had significant effects on microbial communities in the Gulf, but impacts on nitrifying communities in adjacent salt marshes have not been investigated. We studied persistent effects of oil on ammonia-oxidizing archaeal (AOA) and bacterial (AOB) communities and their relationship to nitrification rates and soil properties in Louisiana marshes impacted by the Deepwater Horizon oil spill. Soils were collected at oiled and unoiled sites from Louisiana coastal marshes in July 2012, 2 years after the spill, and analyzed for community differences based on ammonia monooxygenase genes (amoA). Terminal Restriction Fragment Polymorphism and DNA sequence analyses revealed significantly different AOA and AOB communities between the three regions, but few differences were found between oiled and unoiled sites. Community composition of nitrifiers was best explained by differences in soil moisture and nitrogen content. Despite the lack of significant oil effects on overall community composition, we identified differences in correlations of individual populations with potential nitrification rates between oiled and unoiled sites that help explain previously published correlation patterns. Our results suggest that exposure to oil, even 2 years post-spill, led to subtle changes in population dynamics. How, or if, these changes may impact ecosystem function in the marshes, however, remains uncertain