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

Abstract

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.

Ammonia‐oxidizing Bacteria of the Nitrosospira cluster 1 dominate over ammonia‐oxidizing Archaea in oligotrophic surface sediments near the South Atlantic Gyre

“…Half saturation constants (K m ) for betaproteobacterial ammonia oxidation range from 10 to 3300 μM (NH 3 + NH 4 + ) (Stehr et al ., ; Pommerening‐Röser et al ., ; Jiang and Bakken, ; Schramm et al ., ; Bollmann et al ., ). The presence and growth of Nitrosospira cluster 1 in sediments with ammonium concentrations < 10 μM thus likely position them among the AOB with the highest ammonia affinities; adaptation of Nitrosospira cluster 1 to low ammonium was also previously indicated by their increased relative abundance in oligotrophic compared with eutrophic mangrove sediment (Laanbroek et al ., ). Whether Nitrosospira cluster 1 is able to compete for ammonium with high‐affinity AOA, whose K m is in the nM range, cannot be resolved on the basis of our data.…”

Insights into the role of plant on ammonia-oxidizing bacteria and archaea in the mangrove ecosystem

“…In the Mai Po mangrove wetland, Li et al (2011) suggested that it was AOB not AOA communities that were grouped by distances between sampling sites and mangrove trees, which indicated the effect of mangrove trees on AOA and AOB community structures. In a black mangrove in the USA, Laanbroek et al (2012) showed that AOB community structures were shaped by vegetation coverage with which different mangrove habitats were formed. Furthermore, the plant species effect on ammonia-oxidizing community structures was observed in grassland soils as well (Patra et al 2006).…”

“…A case study in mangrove sediments revealed that the effect of mangrove plants on abundances and community structures of AOA and AOB is species dependent . Moreover, Laanbroek et al (2012) showed that soil chemical properties associated with vegetation densities affected community structures of AOB, while an earlier study suggested that variations of nitrification potential between different soils were related to vegetation type rather than the soil physiochemical properties (Wedin and Tilman 1990).…”

Microbiology of wetlands

“…Finally, the paper of Laanbroek et al (2012) introduces the Black mangrove wetlands as a microbial habitat to the reader. The specific focus in this study is on diversity of ammonia-oxidizing Betaproteobacteria , which reflects the changes in hydrology in three different Black mangrove habitats, i.e., locations with dwarf, sparse, and dense trees.…”

“…Notably, these studies address a wide variety of wetland types including rice paddies (Alam and Jia, 2012; Conrad et al, 2012), acidic Sphagnum -dominated peatlands (Bragina et al, 2011; Ivanova and Dedysh, 2012; Kolb and Horn, 2012; Preston et al, 2012; Putkinen et al, 2012; Sun et al, 2012), riparian wetlands (Wang et al, 2012), black mangroves (Laanbroek et al, 2012), superficial aquatic sediments (Gu et al, 2012), salt marshes (Irvine et al, 2012; Lovell and Davis, 2012), and littoral boreal wetlands (Siljanen et al, 2012). …”