Functional control and metabolic integration of stolen organelles in a photosynthetic ciliate.

Stealing prey plastids for metabolic gain is a common phenomenon among protists within aquatic ecosystems.1 Ciliates of the Mesodinium rubrum species complex are unique in that they also steal a transcriptionally active but non-dividing prey nucleus, the kleptokaryon, from certain cryptophytes.2 The kleptokaryon enables full control and replication of kleptoplastids but has a half-life of about 10 days.2 Once the kleptokaryon is lost, the ciliate experiences a slow loss of photosynthetic metabolism and eventually death.2,3,4 This transient ability to function phototrophically allows M. rubrum to form productive blooms in coastal waters.5,6,7,8 Here, we show, using multi-omics approaches, that an Antarctic strain of the ciliate not only depends on stolen Geminigera cryophila organelles for photosynthesis but also for anabolic synthesis of fatty acids, amino acids, and other essential macromolecules. Transcription of diverse pathways was higher in the kleptokaryon than that in G. cryophila, and many increased in higher light. Proteins of major biosynthetic pathways were found in greater numbers in the kleptokaryon relative to M. rubrum, implying anabolic dependency on foreign metabolism. We show that despite losing transcriptional control of the kleptokaryon, M. rubrum regulates kleptoplastid pigments with changing light, implying an important role for post-transcriptional control. These findings demonstrate that the integration of foreign organelles and their gene and protein expression, energy metabolism, and anabolism occur in the absence of a stable endosymbiotic association. Our results shed light on potential events early in the process of complex plastid acquisition and broaden our understanding of symbiogenesis.

Adaptive responses of marine diatoms to zinc scarcity and ecological implications.

Scarce dissolved surface ocean concentrations of the essential algal micronutrient zinc suggest that Zn may influence the growth of phytoplankton such as diatoms, which are major contributors to marine primary productivity. However, the specific mechanisms by which diatoms acclimate to Zn deficiency are poorly understood. Using global proteomic analysis, we identified two proteins (ZCRP-A/B, Zn/Co Responsive Protein A/B) among four diatom species that became abundant under Zn/Co limitation. Characterization using reverse genetic techniques and homology data suggests putative Zn/Co chaperone and membrane-bound transport complex component roles for ZCRP-A (a COG0523 domain protein) and ZCRP-B, respectively. Metaproteomic detection of ZCRPs along a Pacific Ocean transect revealed increased abundances at the surface (<200 m) where dZn and dCo were scarcest, implying Zn nutritional stress in marine algae is more prevalent than previously recognized. These results demonstrate multiple adaptive responses to Zn scarcity in marine diatoms that are deployed in low Zn regions of the Pacific Ocean.

Dynamic diel proteome and daytime nitrogenase activity supports buoyancy in the cyanobacterium Trichodesmium.

Cyanobacteria of the genus Trichodesmium provide about 80 Tg of fixed nitrogen to the surface ocean per year and contribute to marine biogeochemistry, including the sequestration of carbon dioxide. Trichodesmium fixes nitrogen in the daylight, despite the incompatibility of the nitrogenase enzyme with oxygen produced during photosynthesis. While the mechanisms protecting nitrogenase remain unclear, all proposed strategies require considerable resource investment. Here we identify a crucial benefit of daytime nitrogen fixation in Trichodesmium spp. that may counteract these costs. We analysed diel proteomes of cultured and field populations of Trichodesmium in comparison with the marine diazotroph Crocosphaera watsonii WH8501, which fixes nitrogen at night. Trichodesmium's proteome is extraordinarily dynamic and demonstrates simultaneous photosynthesis and nitrogen fixation, resulting in balanced particulate organic carbon and particulate organic nitrogen production. Unlike Crocosphaera, which produces large quantities of glycogen as an energy store for nitrogenase, proteomic evidence is consistent with the idea that Trichodesmium reduces the need to produce glycogen by supplying energy directly to nitrogenase via soluble ferredoxin charged by the photosynthesis protein PsaC. This minimizes ballast associated with glycogen, reducing cell density and decreasing sinking velocity, thus supporting Trichodesmium's niche as a buoyant, high-light-adapted colony forming cyanobacterium. To occupy its niche of simultaneous nitrogen fixation and photosynthesis, Trichodesmium appears to be a conspicuous consumer of iron, and has therefore developed unique iron-acquisition strategies, including the use of iron-rich dust. Particle capture by buoyant Trichodesmium colonies may increase the residence time and degradation of mineral iron in the euphotic zone. These findings describe how cellular biochemistry defines and reinforces the ecological and biogeochemical function of these keystone marine diazotrophs.

Why Environmental Biomarkers Work: Transcriptome-Proteome Correlations and Modeling of Multistressor Experiments in the Marine Bacterium Trichodesmium.

Ocean microbial communities are important contributors to the global biogeochemical reactions that sustain life on Earth. The factors controlling these communities are being increasingly explored using metatranscriptomic and metaproteomic environmental biomarkers. Using published proteomes and transcriptomes from the abundant colony-forming cyanobacterium Trichodesmium (strain IMS101) grown under varying Fe and/or P limitation in low and high CO2, we observed robust correlations of stress-induced proteins and RNAs (i.e., involved in transport and homeostasis) that yield useful information on the nutrient status under low and/or high CO2. Conversely, transcriptional and translational correlations of many other central metabolism pathways exhibit broad discordance. A cellular RNA and protein production/degradation model demonstrates how biomolecules with small initial inventories, such as environmentally responsive proteins, achieve large increases in fold-change units as opposed to those with a higher basal expression and inventory such as metabolic systems. Microbial cells, due to their immersion in the environment, tend to show large adaptive responses in both RNA and protein that result in transcript-protein correlations. These observations and model results demonstrate multi-omic coherence for environmental biomarkers and provide the underlying mechanism for those observations, supporting the promise for global application in detecting responses to environmental stimuli in a changing ocean.