No abstract

The SAR11 Alphaproteobacteria are the most abundant heterotrophs in the oceans and are believed to play a major role in mineralizing marine dissolved organic carbon. Their genomes are among the smallest known for free-living heterotrophic cells, raising questions about how they successfully utilize complex organic matter with a limited metabolic repertoire. Here we show that conserved genes in SAR11 subgroup Ia (Candidatus Pelagibacter ubique) genomes encode pathways for the oxidation of a variety of one-carbon compounds and methyl functional groups from methylated compounds. These pathways were predicted to produce energy by tetrahydrofolate (THF)-mediated oxidation, but not to support the net assimilation of biomass from C1 compounds. Measurements of cellular ATP content and the oxidation of 14C-labeled compounds to 14CO2 indicated that methanol, formaldehyde, methylamine, and methyl groups from glycine betaine (GBT), trimethylamine (TMA), trimethylamine N-oxide (TMAO), and dimethylsulfoniopropionate (DMSP) were oxidized by axenic cultures of the SAR11 strain Ca. P. ubique HTCC1062. Analyses of metagenomic data showed that genes for C1 metabolism occur at a high frequency in natural SAR11 populations. In short term incubations, natural communities of Sargasso Sea microbial plankton expressed a potential for the oxidation of 14C-labeled formate, formaldehyde, methanol and TMAO that was similar to cultured SAR11 cells and, like cultured SAR11 cells, incorporated a much larger percentage of pyruvate and glucose (27–35%) than of C1 compounds (2–6%) into biomass. Collectively, these genomic, cellular and environmental data show a surprising capacity for demethylation and C1 oxidation in SAR11 cultures and in natural microbial communities dominated by SAR11, and support the conclusion that C1 oxidation might be a significant conduit by which dissolved organic carbon is recycled to CO2 in the upper ocean.

Phytoplankton physiology is dynamic and highly responsive to the environment. Phytoplankton acclimate to changing environmental conditions by a complex reallocation of carbon and energy through metabolic pathways to optimize growth. Considering the tremendous diversity of phytoplankton, it is not surprising that different phytoplankton taxa use different strategies to partition carbon and energy resources. It has therefore been satisfying to discover that general principles of energetic stoichiometry appear to govern these complex processes and can be broadly applied to interpret phytoplankton distributions, productivity, and food web dynamics. The expectation of future changes in aquatic environments brought on by climate change warrants gathering knowledge about underlying patterns of photosynthetic energy allocation and their impacts on community structure and ecosystem productivity.

Characterization of physiological variability in phytoplankton photosynthetic efficiencies is one of the greatest challenges in assessing ocean net primary production (NPP) from remote sensing of surface chlorophyll (Chl). Nutrient limitation strongly influences phytoplankton intracellular pigmentation, but its impact on Chl-specific NPP (NPP(*)) is debated. We monitored six indices of photosynthetic activity in steady-state Dunaliella tertiolecta cultures over a range of nitrate-limited growth rates (μ), including photosynthetic efficiency of PSII (F(v)/F(m)), O(2)-based gross and net production, 20 min and 24 h carbon assimilation, and carbon- and μ-based NPP. Across all growth rates, O(2)-based Chl-specific gross primary production (GPP(*)(O(2))), NPP(*), and F(v)/F(m) were constant. GPP(*)(O(2)) was 3.3 times greater than NPP(*). In stark contrast, Chl-specific short-term C fixation showed clear linear dependence on μ, reflecting differential allocation of photosynthate between short-lived C products and longer-term storage products. Indeed, (14)C incorporation into carbohydrates was five times greater in cells growing at 1.2 day(-1) than 0.12 day(-1). These storage products are catabolized for ATP and reductant generation within the period of a cell cycle. The relationship between Chl-specific gross and net O(2) production, short-term (14)C-uptake, NPP(*), and growth rate reflects cellular-level regulation of fundamental metabolic pathways in response to nutrient limitation. We conclude that growth rate-dependent photosynthate metabolism bridges the gap between gross and net production and resolves a controversial question regarding nutrient limitation effects on primary production measures.

Phytoplankton growth and productivity relies on light, multiple nutrients and temperature. These combined factors constitute the 'integrated growth environment'. Since their emergence in the Archaean ocean, phytoplankton have experienced dramatic shifts in their integrated growth environment and, in response, evolved diverse mechanisms to maximize growth by optimizing the allocation of photosynthetic resources (ATP and NADPH) among all cellular processes. Consequently, co-limitation has become an omnipresent condition in the global ocean. Here we focus on evolved phytoplankton populations of the contemporary ocean and the varied energetic pathways they employ to solve the optimization problem of resource supply and demand. Central to this discussion is the allocation of reductant formed through photosynthesis, which we propose has the following three primary fates: carbon fixation, direct use and ATP generation. Investment of reductant among these three sinks is tied to cell cycle events, differentially influenced by specific forms of nutrient stress, and a strong determinant of relationships between light-harvesting (pigment), photosynthetic electron transport and carbon fixation. Global implications of optimization are illustrated by deconvolving trends in the 10-year global satellite chlorophyll record into contributions from biomass and physiology, thereby providing a unique perspective on the dynamic nature of surface phytoplankton populations and their link to climate.