Gammaproteobacterial diazotrophs and nifH gene expression in surface waters of the South Pacific Ocean

Abstract

In addition to the cyanobacterial N2-fixers (diazotrophs), there is a high nifH gene diversity of non-cyanobacterial groups present in marine environments, yet quantitative information about these groups is scarce. N2 fixation potential (nifH gene expression), diversity and distributions of the uncultivated diazotroph phylotype γ-24774A11, a putative gammaproteobacterium, were investigated in the western South Pacific Ocean. γ-24774A11 gene copies correlated positively with diazotrophic cyanobacteria, temperature, dissolved organic carbon and ambient O2 saturation, and negatively with depth, chlorophyll a and nutrients, suggesting that carbon supply, access to light or inhibitory effects of DIN may control γ-24774A11 abundances. Maximum nifH gene-copy abundance was 2 × 10(4) l(-1), two orders of magnitude less than that for diazotrophic cyanobacteria, while the median γ-24774A11 abundance, 8 × 10(2) l(-1), was greater than that for the UCYN-A cyanobacteria, suggesting a more homogeneous distribution in surface waters. The abundance of nifH transcripts by γ-24774A11 was greater during the night than during the day, and the transcripts generally ranged from 0-7%, but were up to 26% of all nifH transcripts at each station. The ubiquitous presence and low variability of γ-24774A11 abundances across tropical and subtropical oceans, combined with the consistent nifH expression reported in this study, suggest that γ-24774A11 could be one of the most important heterotrophic (or photoheterotrophic) diazotrophs and may need to be considered in future N budget estimates and models.

Figure 1

Top: temperature along the cruise transect in the surface. Bottom: abundance of γ-24774A11 in the surface as nifH gene copies log (value+1) l⁻¹.

Figure 2

Neighbor-joining nifH phylogenetic tree for the 359 bp nifH gene region with representative sequences from the study. Station numbers and depths are indicated for sequences from this study.

Figure 3

Neighbor-joining nifH phylogenetic tree for γ-24774A11 sequences from this study and other select studies. Sequences from this study include those obtained with γ-24774A11-specific primers. AO, Atlantic Ocean; MS, Mediterranean Sea; NPAC, North Pacific Ocean; Red Sea; SCS, South China Sea; SPOT, San Pedro Ocean Time-Series, Southern California.

Figure 4

Abundance of γ-24774A11 along the study transect as nifH gene copies (log value+1) l⁻¹.

Figure 5

Integrated nifH transcript abundance in the 0–125 m water column (m⁻²) for γ-24774A11, UCYN-A, C. watsonii, Trichodesmium and Het-1.

Figure 6

Proportions of nifH transcripts during the day (top) and at night (bottom) of the five diazotroph phylotypes. The data are based on transcripts per m⁻².