Jayakumar A, O'Mullan GD, Naqvi SWA, Ward BB.. Denitrifying bacterial community composition changes associated with stages of denitrification in oxygen minimum zones. Microb Ecol 58: 350-362

Department of Geosciences, Guyot Hall, Princeton University, Princeton, NJ 08544, USA.
Microbial Ecology (Impact Factor: 3.12). 03/2009; 58(2):350-62. DOI: 10.1007/s00248-009-9487-y
Source: PubMed


Denitrification in the ocean is a major sink for fixed nitrogen in the global N budget, but the process is geographically restricted to a few oceanic regions, including three oceanic oxygen minimum zones (OMZ) and hemipelagic sediments worldwide. Here, we describe the diversity and community composition of microbes responsible for denitrification in the OMZ using polymerase chain reaction, sequence and fragment analysis of clone libraries of the signature genes (nirK and nirS) that encode the enzyme nitrite reductase, responsible for key denitrification transformation steps. We show that denitrifying assemblages vary in space and time and exhibit striking changes in diversity associated with the progression of denitrification from initial anoxia through nitrate depletion. The initial denitrifying assemblage is highly diverse, but succession on the scale of 3-12 days leads to a much less diverse assemblage and dominance by one or a few phylotypes. This progression occurs in the natural environment as well as in enclosed incubations. The emergence of dominants from a vast reservoir of rare types has implications for the maintenance of diversity of the microbial population and suggests that a small number of microbial dominants may be responsible for the greatest rates of transformations involving nitrous oxide and global fixed nitrogen loss. Denitrifying blooms, driven by a few types responding to episodic environmental changes and distributed unevenly in time and space, are consistent with the sampling effect model of diversity-function relationships. Canonical denitrification thus appears to have important parallels with both primary production and nitrogen fixation, which are typically dominated by regionally and temporally restricted blooms that account for a disproportionate share of these processes worldwide.

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    • "Thus, it appears that the nirS-type nitrite-reducing bacteria are more abundant than nirK-encoding bacteria in deepsea subseafloor sediments. On the other hand, it has been suggested that the diversity of nitrite reducers at a given location may be high during the initial stage of nitrite removal (high ratio of nitrate/nitrite), but lower in later stages of the process when most of the available nitrate/ nitrite is exhausted (Jayakumar et al., 2009). If this holds true for deep-ocean subseafloor sediments, more nitrite reducers are expected at site 401, where the nitrate/nitrite ratio was the highest among all sites in this study (Fig. 1). "

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    • "Further concerns arising from OMZ expansion include a historic association with massive marine extinction events (Kiehl and Shields, 2005). Oxygen-deficient conditions associated with OMZs stress mobile macroorganisms , leading these regions to be dominated by Bacterial and Archaeal species (Stevens and Ulloa, 2008; Jayakumar et al., 2009; Belmar et al., 2011; Stewart et al., 2012). In OMZs, Bacteria and Archaea carry a diverse genetic repertoire which allows the use of alternative electron donors and acceptors during energy metabolism. "
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    ABSTRACT: Oxygen minimum zones (OMZs) are oceanographic features that affect ocean productivity and biodiversity, and contribute to ocean nitrogen loss and greenhouse gas emissions. Here we describe the viral communities associated with the Eastern Tropical South Pacific (ETSP) OMZ off Iquique, Chile for the first time through abundance estimates and viral metagenomic analysis. The viral-to-microbial ratio (VMR) in the ETSP OMZ fluctuated in the oxycline and declined in the anoxic core to below one on several occasions. The number of viral genotypes (unique genomes as defined by sequence assembly) ranged from 2040 at the surface to 98 in the oxycline, which is the lowest viral diversity recorded to date in the ocean. Within the ETSP OMZ viromes, only 4.95% of genotypes were shared between surface and anoxic core viromes using reciprocal BLASTn sequence comparison. ETSP virome comparison with surface marine viromes (Sargasso Sea, Gulf of Mexico, Kingman Reef, Chesapeake Bay) revealed a dissimilarity of ETSP OMZ viruses to those from other oceanic regions. From the 1.4 million non-redundant DNA sequences sampled within the altered oxygen conditions of the ETSP OMZ, more than 97.8% were novel. Of the average 3.2% of sequences that showed similarity to the SEED non-redundant database, phage sequences dominated the surface viromes, eukaryotic virus sequences dominated the oxycline viromes, and phage sequences dominated the anoxic core viromes. The viral community of the ETSP OMZ was characterized by fluctuations in abundance, taxa and diversity across the oxygen gradient. The ecological significance of these changes was difficult to predict; however, it appears that the reduction in oxygen coincides with an increased shedding of eukaryotic viruses in the oxycline, and a shift to unique viral genotypes in the anoxic core.
    Environmental Microbiology 09/2012; 14(11):3043-65. DOI:10.1111/j.1462-2920.2012.02891.x · 6.20 Impact Factor
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    • "Anammox organisms have now been documented in many water column marine oxygen minimum zones (OMZs), and isotope labeling experiments have even shown in some cases a complete lack of denitrification (Schmid et al., 2007; Jensen et al., 2008; Lam et al., 2009). Other labeling studies have pointed towards a dominant contribution from denitrifiers (Ward et al., 2009), while DNA-based methods have suggested the potential for considerable variation in levels of heterotrophic denitrification (Jayakumar et al., 2009a). Conclusions regarding the dominance of one pathway over the other have thus been varied and conflicting (Lam et al., 2007; Schmid et al., 2007; Fuchsman et al., 2008; Lam et al., 2009; Ward et al., 2009; Bulow et al., 2010; Jensen et al., 2011). "
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    ABSTRACT: After the discovery of ANaerobic AMMonium OXidation (anammox) in the environment, the role of heterotrophic denitrification as the main marine pathway for fixed N loss has been questioned. A 3 part, 15 month time series investigating nitrite reductase (nirS) mRNA transcripts at a single location in the Black Sea was conducted in order to better understand the activity of anammox and denitrifying bacteria. Here we show that both of these groups were active, as well as being concurrent in the lower suboxic zone over this time span. Their distributions, however, differed in that only expression of denitrification-type nirS was seen in the upper suboxic zone, where geochemistry was variable. Depth profiles covering the suboxic zone showed that the four groups of anammox-type sequences were expressed consistently in the lower suboxic zone, and were consistent with anammox 16 S rDNA gene profiles. By contrast, denitrifier-type nirS sequence groups were mixed; some groups exhibited consistent expression in the lower suboxic zone, while others appeared less consistent. Co-occurrence of both anammox and denitrifier expression was common and ongoing. Both types of transcripts were also found in samples with low concentrations of sulfide (>2 μM). Six major groups of denitrifier-type nirS transcripts were identified, and several groups of denitrifier-type nirS transcripts were closely related to sequences from the Baltic Sea. An increase in denitrifier-type nirS transcript diversity and depth range in October 2007 corresponded to a small increase in mixed layer net community productivity (NCP) as measured by O(2)/Ar gas ratios, as well as to an increase in N(2) concentrations in the suboxic zone. Taken together, the variations in expression patterns between anammox and denitrification provide one possible explanation as to how near instantaneous rate measurements, such as isotope spike experiments, may regularly detect anammox activity but underreport denitrification.
    Frontiers in Microbiology 07/2012; 3:256. DOI:10.3389/fmicb.2012.00256 · 3.99 Impact Factor
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