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

Molecular and Cellular Biology Program, Oregon State University, Corvallis, OR 97331, USA.
The ISME Journal (Impact Factor: 9.27). 10/2008; 3(1):93-105. DOI: 10.1038/ismej.2008.83
Source: PubMed

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.

Download full-text


Available from: Carrie D Nicora, Jun 27, 2015
  • Source
    [Show abstract] [Hide abstract]
    ABSTRACT: Marine microbial communities provide much of the energy upon which all higher trophic levels depend, particularly in open-ocean and oligotrophic systems, and play a pivotal role in biogeochemical cycling. How and why species are distributed in the global oceans, and whether net ecosystem function can be accurately predicted from community composition are fundamental questions for marine scientists. Many of the most abundant clades of marine bacteria, including the Prochlorococcus, Synechococcus, SAR11, SAR86 and Roseobacter, have a very broad, if not a cosmopolitan distribution. However this is not reflected in an underlying genetic identity. Rather, widespread distribution in these organisms is achieved by the existence of closely related but discrete ecotypes that display niche adaptations. Closely related ecotypes display specific nutritional or energy generating mechanisms and are adapted to different physical parameters including temperature, salinity, and hydrostatic pressure. Furthermore, biotic phenomena such as selective grazing and viral loss contribute to the success or failure of ecotypes allowing some to compete effectively in particular marine provinces but not in others. An additional layer of complexity is added by ocean currents and hydrodynamic specificity of water body masses that bound microbial dispersal and immigration. These vary in space and time with respect to intensity and direction, making the definition of large biogeographic provinces problematic. A deterministic theory aimed at understanding how all these factors shape microbial life in the oceans can only proceed through analysis of microbial traits, rather than pure phylogenetic assessments. Trait based approaches seek mechanistic explanations for the observed temporal and spatial patterns. This review will present successful recent advances in phylogenetic and trait based biogeographic analyses in some of the most abundant marine taxa.
    Marine Genomics 06/2014; 15. DOI:10.1016/j.margen.2014.03.002 · 1.97 Impact Factor
  • Source
    [Show abstract] [Hide abstract]
    ABSTRACT: Metaproteomics is a new field within the 'omics' science which investigates protein expression from a complex biological system and provides direct evidence of physiological and metabolic activities. Characterization of the metaproteome will enhance our understanding of the microbial world and link microbial communities to ecological functions. Recently, the availability of extensive metagenomic sequences from various marine microbial communities has extended the postgenomic era to the field of oceanography. Although still in its infancy, metaproteomics has shown its powerful potential with regard to functional gene expression within microbial habitats and their interactions with the ambient environment as well as their biogeochemical functions. However, the application of metaproteomic approaches to complex marine samples still faces considerable challenges. This review summarizes the recent progress in marine metaproteomics and discusses the limitations of and perspectives for this approach in the study of the marine ecosystem.
    Journal of proteomics 01/2014; 97:27-35. DOI:10.1016/j.jprot.2013.08.024 · 3.93 Impact Factor
  • Source
    [Show abstract] [Hide abstract]
    ABSTRACT: In this study, we used comparative metaproteomics to investigate the metabolic activity of microbial plankton inhabiting a seasonally hypoxic basin in the Northwest Atlantic Ocean (Bedford Basin). From winter to spring, we observed a seasonal increase in high-affinity membrane transport proteins involved in scavenging of organic substrates; Rhodobacterales transporters were strongly associated with the spring phytoplankton bloom, whereas SAR11 transporters were abundant in the underlying waters. A diverse array of transporters for organic compounds were similar to the SAR324 clade, revealing an active heterotrophic lifestyle in coastal waters. Proteins involved in methanol oxidation (from the OM43 clade) and carbon monoxide (from a wide variety of bacteria) were identified throughout Bedford Basin. Metabolic niche partitioning between the SUP05 and ARCTIC96BD-19 clades, which together comprise the Gamma-proteobacterial sulfur oxidizers group was apparent. ARCTIC96BD-19 proteins involved in the transport of organic compounds indicated that in productive coastal waters this lineage tends toward a heterotrophic metabolism. In contrast, the identification of sulfur oxidation proteins from SUP05 indicated the use of reduced sulfur as an energy source in hypoxic bottom water. We identified an abundance of Marine Group I Thaumarchaeota proteins in the hypoxic deep layer, including proteins for nitrification and carbon fixation. No transporters for organic compounds were detected among the thaumarchaeal proteins, suggesting a reliance on autotrophic carbon assimilation. In summary, our analyses revealed the spatiotemporal structure of numerous metabolic activities in the coastal ocean that are central to carbon, nitrogen and sulfur cycling in the sea.The ISME Journal advance online publication, 9 January 2014; doi:10.1038/ismej.2013.234.
    The ISME Journal 01/2014; DOI:10.1038/ismej.2013.234 · 9.27 Impact Factor