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1. Long-Term m5C Methylome Dynamics Parallel Phenotypic Adaptation in the Cyanobacterium Trichodesmium

   https://doi.org/10.1093/molbev/msaa256  

   Walworth, Nathan G ; Lee, Michael D ; Dolzhenko, Egor ; Fu, Fei-Xue ; Smith, Andrew D ; Webb, Eric A ; Hutchins, David A ( October 2020 , Molecular Biology and Evolution)

   Abstract A major challenge in modern biology is understanding how the effects of short-term biological responses influence long-term evolutionary adaptation, defined as a genetically determined increase in fitness to novel environments. This is particularly important in globally important microbes experiencing rapid global change, due to their influence on food webs, biogeochemical cycles, and climate. Epigenetic modifications like methylation have been demonstrated to influence short-term plastic responses, which ultimately impact long-term adaptive responses to environmental change. However, there remains a paucity of empirical research examining long-term methylation dynamics during environmental adaptation in nonmodel, ecologically important microbes. Here, we show the first empirical evidence in a marine prokaryote for long-term m5C methylome modifications correlated with phenotypic adaptation to CO2, using a 7-year evolution experiment (1,000+ generations) with the biogeochemically important marine cyanobacterium Trichodesmium. We identify m5C methylated sites that rapidly changed in response to high (750 µatm) CO2 exposure and were maintained for at least 4.5 years of CO2 selection. After 7 years of CO2 selection, however, m5C methylation levels that initially responded to high-CO2 returned to ancestral, ambient CO2 levels. Concurrently, high-CO2 adapted growth and N2 fixation rates remained significantly higher than those of ambient CO2 adapted cell lines irrespective of CO2 concentration,more »a trend consistent with genetic assimilation theory. These data demonstrate the maintenance of CO2-responsive m5C methylation for 4.5 years alongside phenotypic adaptation before returning to ancestral methylation levels. These observations in a globally distributed marine prokaryote provide critical evolutionary insights into biogeochemically important traits under global change.« less
2. Warming Iron-Limited Oceans Enhance Nitrogen Fixation and Drive Biogeographic Specialization of the Globally Important Cyanobacterium Crocosphaera

   https://doi.org/10.3389/fmars.2021.628363  

   Yang, Nina ; Merkel, Carlin A. ; Lin, Yu-An ; Levine, Naomi M. ; Hawco, Nicholas J. ; Jiang, Hai-Bo ; Qu, Ping-Ping ; DeMers, Michelle A. ; Webb, Eric A. ; Fu, Fei-Xue ; et al ( February 2021 , Frontiers in Marine Science)

   Primary productivity in the nutrient-poor subtropical ocean gyres depends on new nitrogen inputs from nitrogen fixers that convert inert dinitrogen gas into bioavailable forms. Temperature and iron (Fe) availability constrain marine nitrogen fixation, and both are changing due to anthropogenic ocean warming. We examined the physiological responses of the globally important marine nitrogen fixer, Crocosphaera watsonii across its full thermal range as a function of iron availability. At the lower end of its thermal range, from 22 to 27°C, Crocosphaera growth, nitrogen fixation, and Nitrogen-specific Iron Use Efficiencies (N-IUEs, mol N fixed hour –1 mol Fe –1 ) increased with temperature. At an optimal growth temperature of 27°C, N-IUEs were 66% higher under iron-limited conditions than iron-replete conditions, indicating that low-iron availability increases metabolic efficiency. However, Crocosphaera growth and function decrease from 27 to 32°C, temperatures that are predicted for an increasing fraction of tropical oceans in the future. Altogether, this suggests that Crocosphaera are well adapted to iron-limited, warm waters, within prescribed limits. A model incorporating these results under the IPCC RCP 8.5 warming scenario predicts that Crocosphaera N-IUEs could increase by a net 47% by 2100, particularly in higher-latitude waters. These results contrast with published responses of anothermore »dominant nitrogen fixer ( Trichodesmium ), with predicted N-IUEs that increase most in low-latitude, tropical waters. These models project that differing responses of Crocosphaera and Trichodesmium N-IUEs to future warming of iron-limited oceans could enhance their current contributions to global marine nitrogen fixation with rates increasing by ∼91 and ∼22%, respectively, thereby shifting their relative importance to marine new production and also intensifying their regional divergence. Thus, interactive temperature and iron effects may profoundly transform existing paradigms of nitrogen biogeochemistry and primary productivity in open ocean regimes.« less
3. Co-occurrence of Fe and P stress in natural populations of the marine diazotroph <i>Trichodesmium</i>

   https://doi.org/10.5194/bg-17-2537-2020  

   Held, Noelle A. ; Webb, Eric A. ; McIlvin, Matthew M. ; Hutchins, David A. ; Cohen, Natalie R. ; Moran, Dawn M. ; Kunde, Korinna ; Lohan, Maeve C. ; Mahaffey, Claire ; Woodward, E. Malcolm ; et al ( January 2020 , Biogeosciences)

   Abstract. Trichodesmium is a globally important marine microbe that provides fixednitrogen (N) to otherwise N-limited ecosystems. In nature, nitrogen fixationis likely regulated by iron or phosphate availability, but the extent andinteraction of these controls are unclear. From metaproteomics analysesusing established protein biomarkers for nutrient stress, we foundthat iron–phosphate co-stress is the norm rather than the exception for Trichodesmium colonies in theNorth Atlantic Ocean. Counterintuitively, the nitrogenase enzyme was moreabundant under co-stress as opposed to single nutrient stress. This isconsistent with the idea that Trichodesmium has a specific physiological state duringnutrient co-stress. Organic nitrogen uptake was observed and occurredsimultaneously with nitrogen fixation. The quantification of the phosphate ABCtransporter PstA combined with a cellular model of nutrient uptake suggestedthat Trichodesmium is generally confronted by the biophysical limits of membrane spaceand diffusion rates for iron and phosphate acquisition in the field. Colonyformation may benefit nutrient acquisition from particulate and organicsources, alleviating these pressures. The results highlight that topredict the behavior of Trichodesmium, both Fe and P stress must be evaluatedsimultaneously.
4. Physiological and biochemical responses of <i>Emiliania huxleyi</i> to ocean acidification and warming are modulated by UV radiation

   https://doi.org/10.5194/bg-16-561-2019  

   Tong, Shanying ; Hutchins, David A. ; Gao, Kunshan ( January 2019 , Biogeosciences)

   Abstract. Marine phytoplankton such as bloom-forming, calcite-producingcoccolithophores, are naturally exposed to solar ultraviolet radiation (UVR,280–400nm) in the ocean's upper mixed layers. Nevertheless, the effects ofincreasing carbon dioxide (CO₂)-induced ocean acidification and warming have rarelybeen investigated in the presence of UVR. We examined calcification andphotosynthetic carbon fixation performance in the most cosmopolitancoccolithophorid, Emiliania huxleyi, grown under high(1000µatm, HC; pH_T: 7.70) and low (400µatm,LC; pH_T: 8.02) CO₂ levels, at 15^∘C,20^∘C and 24^∘C with or without UVR. The HCtreatment did not affect photosynthetic carbon fixation at 15^∘C,but significantly enhanced it with increasing temperature. Exposure to UVRinhibited photosynthesis, with higher inhibition by UVA (320–395nm) thanUVB (295–320nm), except in the HC and 24^∘C-grown cells, in whichUVB caused more inhibition than UVA. A reduced thickness of the coccolith layerin the HC-grown cells appeared to be responsible for the UV-inducedinhibition, and an increased repair rate of UVA-derived damage in theHC–high-temperature grown cells could be responsible for lowered UVA-induced inhibition.While calcification was reduced with elevated CO₂ concentration,exposure to UVB or UVA affected the process differentially, with the formerinhibiting it and the latter enhancing it. UVA-induced stimulationmore »of calcification washigher in the HC-grown cells at 15 and 20^∘C, whereas at24^∘C observed enhancement was not significant. The calcificationto photosynthesis ratio (Cal∕Pho ratio) was lower in the HC treatment,and increasing temperature also lowered the value. However, at 20 and24^∘C, exposure to UVR significantly increased the Cal∕Phoratio, especially in HC-grown cells, by up to 100%. This implies thatUVR can counteract the negative effects of the “greenhouse” treatment onthe Cal∕Pho ratio; hence, UVR may be a key stressor when considering theimpacts of future greenhouse conditions on E. huxleyi.

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5. Utilizing the Drake Passage Time-series to understand variability and change in subpolar Southern Ocean <i>p</i>CO₂

   https://doi.org/10.5194/bg-15-3841-2018  

   Fay, Amanda R. ; Lovenduski, Nicole S. ; McKinley, Galen A. ; Munro, David R. ; Sweeney, Colm ; Gray, Alison R. ; Landschützer, Peter ; Stephens, Britton B. ; Takahashi, Taro ; Williams, Nancy ( January 2018 , Biogeosciences)

   Abstract. The Southern Ocean is highly under-sampled for the purpose of assessing total carbon uptake and its variability. Since this region dominates the mean global ocean sink for anthropogenic carbon, understanding temporal change is critical. Underway measurements of pCO2 collected as part of the Drake Passage Time-series (DPT) program that began in 2002 inform our understanding of seasonally changing air–sea gradients in pCO2, and by inference the carbon flux in this region. Here, we utilize available pCO2 observations to evaluate how the seasonal cycle, interannual variability, and long-term trends in surface ocean pCO2 in the Drake Passage region compare to that of the broader subpolar Southern Ocean. Our results indicate that the Drake Passage is representative of the broader region in both seasonality and long-term pCO2 trends, as evident through the agreement of timing and amplitude of seasonal cycles as well as trend magnitudes both seasonally and annually. The high temporal density of sampling by the DPT is critical to constraining estimates of the seasonal cycle of surface pCO2 in this region, as winter data remain sparse in areas outside of the Drake Passage. An increase in winter data would aid in reduction of uncertainty levels. On average over themore »period 2002–2016, data show that carbon uptake has strengthened with annual surface ocean pCO2 trends in the Drake Passage and the broader subpolar Southern Ocean less than the global atmospheric trend. Analysis of spatial correlation shows Drake Passage pCO2 to be representative of pCO2 and its variability up to several hundred kilometers away from the region. We also compare DPT data from 2016 and 2017 to contemporaneous pCO2 estimates from autonomous biogeochemical floats deployed as part of the Southern Ocean Carbon and Climate Observations and Modeling project (SOCCOM) so as to highlight the opportunity for evaluating data collected on autonomous observational platforms. Though SOCCOM floats sparsely sample the Drake Passage region for 2016–2017 compared to the Drake Passage Time-series, their pCO2 estimates fall within the range of underway observations given the uncertainty on the estimates. Going forward, continuation of the Drake Passage Time-series will reduce uncertainties in Southern Ocean carbon uptake seasonality, variability, and trends, and provide an invaluable independent dataset for post-deployment assessment of sensors on autonomous floats. Together, these datasets will vastly increase our ability to monitor change in the ocean carbon sink.« less