Contribution of SAR11 bacteria to dissolved dimethylsulfoniopropionate and amino acid uptake in the North Atlantic ocean

Abstract

SAR11 bacteria are abundant in marine environments, often accounting for 35% of total prokaryotes in the surface ocean, but little is known about their involvement in marine biogeochemical cycles. Previous studies reported that SAR11 bacteria are very small and potentially have few ribosomes, indicating that SAR11 bacteria could have low metabolic activities and could play a smaller role in the flux of dissolved organic matter than suggested by their abundance. To determine the ecological activity of SAR11 bacteria, we used a combination of microautoradiography and fluorescence in situ hybridization (Micro-FISH) to measure assimilation of (3)H-amino acids and [(35)S]dimethylsulfoniopropionate (DMSP) by SAR11 bacteria in the coastal North Atlantic Ocean and the Sargasso Sea. We found that SAR11 bacteria were often abundant in surface waters, accounting for 25% of all prokaryotes on average. SAR11 bacteria were typically as large as, if not larger than, other prokaryotes. Additionally, more than half of SAR11 bacteria assimilated dissolved amino acids and DMSP, whereas about 40% of other prokaryotes assimilated these compounds. Due to their high abundance and activity, SAR11 bacteria were responsible for about 50% of amino acid assimilation and 30% of DMSP assimilation in surface waters. The contribution of SAR11 bacteria to amino acid assimilation was greater than would be expected based on their overall abundance, implying that SAR11 bacteria outcompete other prokaryotes for these labile compounds. These data suggest that SAR11 bacteria are highly active and play a significant role in C, N, and S cycling in the ocean.

FIG. 1.

Stations sampled in the Gulf of Maine, Sargasso Sea, and North Carolina coast in April 2002. Samples were collected at 11 separate stations, although stations 2 and 3, 7 and 8, and 10 and 12 are not distinguishable at this scale.

FIG. 2.

Abundance of bacteria and SAR11 bacteria at 10 m in the Gulf of Maine, mid-Atlantic (M.A.), Sargasso Sea, and North Carolina (N.C.) coastal waters. The abundance of bacteria detected by general bacterial probes (open bars) and SAR11 bacteria (filled bars) is expressed as a percentage of total prokaryotes (DAPI-positive cells). Error bars represent the standard errors of 30 fields of view. These data are from FISH analyses, not the microautoradiography preparations.

FIG. 3.

Percentage of SAR11 bacteria and all other prokaryotes assimilating dissolved free amino acids (A) and dissolved DMSP (B) in the Gulf of Maine, the Sargasso Sea, and North Carolina coastal waters. Statistically significant differences (t test; P < 0.05) between SAR11 bacteria and other prokaryotes are indicated (*). Error bars represent the standard errors of 30 fields of view.

FIG. 4.

Frequency distribution of silver grain cluster areas associated with SAR11 bacteria (A) and all other prokaryotes (B) assimilating amino acids at station 8 in the Sargasso Sea. Silver grain areas were grouped into bins at 0.25-μm² increments. These distributions are representative of those from all other stations where amino acid assimilation was measured.

FIG. 5.

Contribution of SAR11 bacteria to the assimilation of dissolved free amino acids and DMSP. Abundance of SAR11 bacteria in the amino acid- and DMSP-assimilating community is plotted against abundance of SAR11 bacteria in the total prokaryote community (A and C). Percentage of total silver grain area associated with SAR11 bacteria is plotted against the abundance of SAR11 bacteria in the total prokaryote community (B and D). Error bars represent the standard errors of 30 fields of view.