Abundances and distributions of the dominant nifH phylotypes in the Northern Atlantic Ocean

Abstract

Understanding the factors that influence the distribution and abundance of marine diazotrophs is important in order to assess their role in the oceanic nitrogen cycle. Environmental DNA samples from four cruises to the North Atlantic Ocean, covering a sampling area of 0 degrees N to 42 degrees N and 67 degrees W to 13 degrees W, were analyzed for the presence and amount of seven nifH phylotypes using real-time quantitative PCR and TaqMan probes. The cyanobacterial phylotypes dominated in abundance (94% of all nifH copies detected) and were the most widely distributed. The filamentous cyanobacterial type, which included both Trichodesmium and Katagnymene, was the most abundant (51%), followed by group A, an uncultured unicellular cyanobacterium (33%), and gamma A, an uncultured gammaproteobacterium (6%). Group B, unicellular cyanobacterium Crocosphaera, and group C Cyanothece-like phylotypes were not often detected (6.9% and 2.3%, respectively), but where present, could reach high concentrations. Gamma P, another uncultured gammaproteobacterium, was seldom detected (0.5%). Water temperature appeared to influence the distribution of many nifH phylotypes. Very high (up to 1 x 10(6) copies liter(-1)) nifH concentrations of group A were detected in the eastern basin (25 to 17 degrees N, 27 to 30 degrees W), where the temperature ranged from 20 to 23 degrees C. The highest concentrations of filamentous phylotypes were measured between 25 and 30 degrees C. The uncultured cluster III phylotype was uncommon (0.4%) and was associated with mean water temperatures of 18 degrees C. Diazotroph abundance was highest in regions where modeled average dust deposition was between 1 and 2 g/m(2)/year.

FIG. 1.

Total nifH copies liter⁻¹ detected at each station (a) and nifH copies liter⁻¹ of each phylotype in panels b to h were plotted using Ocean Data View (37). Black dots indicate samples with concentrations below the detection limit. Note that the color scale is a log scale. Fil, filamentous; Gam, gamma; Grp, group; CIII, cluster III.

FIG. 2.

Box-whisker plots (black dots, mean; boxes, standard error; bars, 95% confidence interval) show the temperatures where >100 nifH copies liter⁻¹ were detected for all phylotypes in panel a. The mean temperature of all samples (22°C) and the associated standard error are indicated by a black line and dashed line, respectively. Phylotype temperature means which are significantly different from 22°C (P < 0.05, Kruskal-Wallis test) are identified by asterisks. Letters signify groups of phylotypes whose temperature means are not significantly different from another group (Mann-Whitney U test). Average filamentous and group A nifH copies liter⁻¹ detected at sample temperatures rounded to the nearest whole degree are displayed in panel b. Error bars indicate the standard error.

FIG. 3.

Separation of stations according to geographical location (a) and physical characteristics (see the supplemental material). Station locations are overlaid on a map of predicted annual dust deposition. The average number of nifH copies liter⁻¹ and standard error from all samples (clear bars) and only surface samples (black bars) in each region are plotted in panel b. Region letters correspond to the panels in Fig. 4. Sonne 152 samples were not plotted because no temperature and salinity data were available.

FIG. 4.

Average concentrations of nifH copies liter⁻¹ by sample temperature (rounded to the nearest whole degree) in each geographic location are shown, with panel letters corresponding to the regions in Fig. 3. ▪, filamentous; □, group A, , group B; , group C; ▥, gamma A; , gamma P; and , cluster III. The numbers of samples for regions a, b, c, d, e, and f are 21, 8, 6, 40, 105, and 96, respectively. Panels e′ and f′ show the average numbers of nifH copies liter⁻¹ from panels e and f without the dominant group A and filamentous phylotypes, respectively.

FIG. 5.

Average concentrations of nifH copies liter⁻¹ for filamentous (▪), group A (□), and all other phylotypes combined (gray square) as a function of estimated annual dust deposition are shown. Average temperatures of each region were 22.3°C (5 to 10 g m⁻² year⁻¹), 24.5°C (2 to 5 g m⁻² year⁻¹), 26.8°C (1 to 2 g m⁻² year⁻¹), and 19.3°C (<1 g m⁻² year⁻¹). The dust deposition map was provided by I. Tegen, using the data from reference .