Seasonal patterns of nitrogen fixation and denitrification in oceanic mangrove habitats

Abstract

Mangrove peat soils are home to a variety of microbial communities that may play a vital role in system-level elemental cycling. We examined rates of nitrogen fixation and denitrification in benthic microbial mats on Twin Cays, Belize, a pair of oceanic mangrove islands. A tree-height gradient across the islands created distinct habitats for benthic microbes. Seawater flushing of the benthos and tree height decreased landward from tall, dense trees on the island fringe through a transition zone of high elevation and intermediate tree heights. In the center of the islands, microbial mats with dense communities of cyanobacteria and purple sulfur bacteria covered the benthic surface of shallow ponds and around dwarf trees. Wet-dry seasonality, tidal cycles and elevation controlled the extent of mat exposure to desiccation and UV radiation. Nitrogen fixation was controlled primarily by the sensitivity of nitrogenase to oxygen inhibition, whereas denitrification was limited by oxidant (nitrate) availability. Diel patterns of nitrogen fixation varied with the type of cyanobacteria dominant in each mat. Dissolved inorganic nitrogen concentration influenced both nitrogen fixation and denitrification rates. Redox conditions contributed to variability in mat nitrogen fixation and denitrification response to nutrient addition, while dissolved organic carbon did not. Microbial mat nitrogen cycling likely contributes to the nutrient (nitrogen and phosphorus) limitation patterns observed in the mangrove trees; in dwarf habitats, mats serve as a source of nitrogen via nitrogen fixation, while in fringe and transition habitats, mats compete with the trees for nitrogen via denitrification.

Nutrient enrichment in tropical wetlands: shifts from autotrophic to heterotrophic nitrogen fixation

“…Research on biological nitrogen (N) fixation and its role in maintaining soil N fertility in wetland ecosystems has focused on coastal wetlands such as salt marshes, mangroves (Pelegri and Twilley 1998;Bagwell and Lovell 2000;Nielsen et al 2001;Tyler et al 2003; Lee and Joye 2006;Moseman 2007), and on rice fields (Eskew et al 1981;Roger and Ladha 1992;Roger 1995). Data from freshwater wetlands, however, are rather limited (Bristow 1973;Tjepkema and Evans 1976;Scott et al 2008;Č erná et al 2009).…”

“…Two types of organisms are often responsible for N fixation in wetlands: autotrophic cyanobacteria, which occur in benthic, floating, or periphytic cyanobacterial mats (Rejmánková and Komárková 2000;Rejmánková et al 2004;Inglett et al 2004Inglett et al , 2009Scott et al 2005Scott et al , 2007Lee and Joye 2006), and heterotophic N fixers in the rhizosphere or in bulk sediments (Moseman 2007;Č erná et al 2009). Autotrophic N fixation prevails in oligotrophic and mesotrophic wetlands where cyanobacterial mats are often the main primary producers because macrophytes are nutrient limited (Rejmánková and Komár-ková 2000;Scott et al 2007).…”

Phylogenetic Diversity of Diazotrophs along an Experimental Nutrient Gradient in Mangrove Sediments

“…Mangrove sediments in our study exhibit a high diversity of the nifH gene with only 12% of the sequenced clones being closely related to clones from other mangrove areas [13,19]. The lack of representatives from the Alpha-Proteobacteria group and common cyanobacteria species found in other mangroves [12,13,19] might reflect differences in either mangrove locations or type of sediment sampled. This indicates some diazotrophs may be partially endemic to geographically distinct mangrove forests, which has important implications in restoration and conservation efforts [20,68,69].…”

“…Sulfate reduction is an important process mediating the majority of the organic matter oxidation in sediments in our study area [75]. It appears that the biogeochemical signatures or microbial processes observed in Belize in previous studies are unique from other mangroves [75] with high rates of N2 fixation and sulfate reduction [12,14,75]. This may be a reflection of sediment composition in our studied area, more typical of oceanic mangrove ecosystems [33], and may offer a unique environment for bacterial communities like nitrogen-fixing sulfate reducers.…”

“…Mangroves ability to conserve nutrients as a whole ecosystem relies largely on the mineralization of organic matter by active microorganisms, an important component for the productivity of the ecosystem [9][10][11]. Diazotrophs (nitrogen fixing bacteria) are a physiologically and phylogenetically diverse microbial group responsible for most nitrogen input in the mangrove ecosystem [12][13][14]. Nitrogen fixation is the second major microbial processes within the mangrove ecosystem, after decomposition of organic matter by sulfate reducing bacteria [10].…”