N2 fixation by unicellular bacterioplankton from the Atlantic and Pacific oceans: phylogeny and in situ rates

Abstract

N2-fixing proteobacteria (alpha and gamma) and unicellular cyanobacteria are common in both the tropical North Atlantic and Pacific oceans. In near-surface waters proteobacterial nifH transcripts were present during both night and day while unicellular cyanobacterial nifH transcripts were present during the nighttime only, suggesting separation of N2 fixation and photosynthesis by unicellular cyanobacteria. Phylogenetic relationships among unicellular cyanobacteria from both oceans were determined after sequencing of a conserved region of 16S ribosomal DNA (rDNA) of cyanobacteria, and results showed that they clustered together, regardless of the ocean of origin. However, sequencing of nifH transcripts of unicellular cyanobacteria from both oceans showed that they clustered separately. This suggests that unicellular cyanobacteria from the tropical North Atlantic and subtropical North Pacific share a common ancestry (16S rDNA) and that potential unicellular N2 fixers have diverged (nifH). N2 fixation rates for unicellular bacterioplankton (including small cyanobacteria) from both oceans were determined in situ according to the acetylene reduction and 15N2 protocols. The results showed that rates of fixation by bacterioplankton can be almost as high as those of fixation by the colonial N2-fixing marine cyanobacteria Trichodesmium spp. in the tropical North Atlantic but that rates are much lower in the subtropical North Pacific.

FIG. 1.

Phylogenetic reconstruction (maximum parsimony) for nifH gene sequences from bacterioplankton in the tropical North Atlantic and subtropical North Pacific oceans. Asterisks indicate sequences obtained as part of this study. Daytime and nighttime transcripts are indicated by open and solid circles, respectively.

FIG. 2.

Summary of phylogenetic reconstruction (maximum parsimony) for 16S rDNA sequences from unicellular cyanobacteria in the tropical North Atlantic and subtropical North Pacific oceans. Asterisks indicate sequences obtained as part of this study.

FIG. 3.

Distribution of average rates of in situ N₂ fixation (picomoles of N liter⁻¹ hour⁻¹) by bacterioplankton by depth for the tropical North Atlantic (solid symbols) and subtropical North Pacific (open symbols). ¹⁵N₂ 24-h incubations in summer 2001 are shown by ▾. Symbols indicate periods of incubations and reading time in gas chromatography: ▴, 1800 to 2200 h; ▪, 2200 to 0200 h; and •, 0200 to 0600 h for spring 2002, tropical North Atlantic; ▵, 1200 to 1800 h; □, 1800 to 2400 h; and ○, 2400 to 0600 h for fall 2002, subtropical North Pacific. Error bars represent standard errors. Only readings where nitrogenase activity was detected are shown.

FIG. 4.

Distribution of average cell counts of unicellular cyanobacteria by depth, in the tropical North Atlantic (solid symbols; ∼2.5 μm) and subtropical North Pacific (open symbols; 3 and 7 μm) oceans. Error bars represent standard errors.