Transport functions dominate the SAR11 metaproteome at low-nutrient extremes in the Sargasso Sea

Abstract

The northwestern Sargasso Sea undergoes annual cycles of productivity with increased production in spring corresponding to periods of upwelling, and oligotrophy in summer and autumn, when the water column becomes highly stratified. The biological productivity of this region is reduced during stratified periods as a result of low concentrations of phosphorus and nitrogen in the euphotic zone. To better understand the mechanisms of microbial survival in this oligotrophic environment, we used capillary liquid chromatography (LC)-tandem mass spectrometry to detect microbial proteins in surface samples collected in September 2005. A total of 2215 peptides that mapped to 236 SAR11 proteins, 1911 peptides that mapped to 402 Prochlorococcus proteins and 2407 peptides that mapped to 404 Synechococcus proteins were detected. Mass spectra from SAR11 periplasmic substrate-binding proteins accounted for a disproportionately large fraction of the peptides detected, consistent with observations that these extremely small cells devote a large proportion of their volume to periplasm. Abundances were highest for periplasmic substrate-binding proteins for phosphate, amino acids, phosphonate, sugars and spermidine. Proteins implicated in the prevention of oxidative damage and protein refolding were also abundant. Our findings support the view that competition for multiple nutrients in oligotrophic systems is extreme, but nutrient flux is sufficient to sustain microbial community activity.

Microbial community gene expression within colonies of the diazotroph, Trichodesmium, from the Southwest Pacific Ocean

“…Consistent with this, there is a transcript encoding an alkaline phosphatase enzyme, which hydrolyzes phosphate from dissolved organic phosphorus, and there are several transcripts encoding exopolyphosphatases (ppX), an enzyme involved in the breakdown of polyphosphate stores. A recent proteome study in the lowphosphorus Sargasso Sea identified phosphate binding and transport, a dominant feature of the SAR11, Prochlorococcus and Synechococcus metaproteome (Sowell et al, 2009). In this study, there are similarly a number of transcripts associated with the high-affinity uptake of phosphate, including pstsS/sphX and a possible pstB transcript in Crocosphaera.…”

Seasonal dynamics of SAR11 populations in the euphotic and mesopelagic zones of the northwestern Sargasso Sea

“…So far the genomic and physiological properties that distinguish the ecotypes of SAR11 have not been reported; most of what is known was determined from the study of coastal isolates from subclade Ia (Giovannoni et al, 2005a;Tripp et al, 2008a, b) and metagenomic and metaproteomic data (Venter et al, 2004;Wilhelm et al, 2007;Sowell et al, 2008). These organisms have the smallest genomes known for free-living heterotrophic cells, an apparent consequence of genome streamlining and reduction driven by the selection for efficient growth in oligotrophic ocean habitats (Giovannoni et al, 2005a).…”

Environmental Shaping of Codon Usage and Functional Adaptation Across Microbial Communities

“…We compared our predictions of gene expression with two available metaproteomic studies that provided abundances of a comparably large number of proteins, the Sargasso Sea metaproteomic study (17) and a functionally (COG) classified subset of the human gut metaproteomic study (18). The predicted expression values based on CU optimization positively correlate with abundance in metaproteomic studies ( …”

“…Even though there is an abundance of available metagenomic data, analogous studies of the whole proteome complement of an environment (17)(18)(19) are in their infancy and their throughput cannot rival that of metagenomics. Therefore, the most accessible approach to define communities at the level of proteome content will in the near future remain (meta)genome-based.…”

“…In contrast to metagenomics, there are only a few metaproteomic studies (i.e. investigations of the total proteomes of microbial communities) (16)(17)(18)(19) owing mostly to the complexity of experimental set-up and a relatively low throughput limited by high experimental costs (16).…”