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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)

   null (Ed.)

   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, 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. 

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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)

   null (Ed.)

   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 another 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. 

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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. 

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4. Interactions between ultraviolet radiation exposure and phosphorus limitation in the marine nitrogen‐fixing cyanobacteria Trichodesmium and Crocosphaera

   https://doi.org/10.1002/lno.11304  

   Zhu, Zhu ; Fu, Feixue ; Qu, Pingping ; Mak, Esther Wing Kwan ; Jiang, Haibo ; Zhang, Ruifeng ; Zhu, Zhuoyi ; Gao, Kunshan ; Hutchins, David A. ( August 2019 , Limnology and Oceanography)

   Increased stratification and mixed layer shoaling of the surface ocean resulting from warming can lead to exposure of marine dinitrogen (N₂)‐fixing cyanobacteria to higher levels of inhibitory ultraviolet (UV) radiation. These same processes also reduce vertically advected supplies of the potentially limiting nutrient phosphorus (P) to N₂fixers. It is currently unknown how UV inhibition and P limitation interact to affect the biogeochemical cycles of nitrogen and carbon in these biogeochemically critical microbes. We investigated the responses of the important and widespread marine N₂‐fixing cyanobacteriaCrocosphaera(strain WH0005) andTrichodesmium(strains IMS 101 and GBR) to UV‐A and UV‐B under P‐replete and P‐limited conditions. Growth, N₂fixation, and carbon dioxide (CO₂) fixation rates ofTrichodesmiumIMS 101 andCrocosphaerawere negatively affected by UV exposure. This inhibition was greater forTrichodesmiumIMS 101 than forCrocosphaera, which fixes N₂only during the night and so avoids direct UV damage. Negative effects of UV on both IMS 101 andCrocosphaerawere less in P‐limited cultures than in P‐replete cultures. In contrast, no UV inhibition was observed in GBR, regardless of P availability. UV inhibition was related to different amounts of UV‐absorbing compounds produced by these isolates. Responses to UV radiation and P availability interactions were taxon‐specific, but our results indicated that in general, UV radiation effects onTrichodesmiumandCrocosphaerarange from negative to neutral. UV inhibition and its interactions with P limitation may thus have a substantial influence on the present day and future nitrogen and carbon cycles of the ocean.

    

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5. Experimental evolution of phytoplankton fatty acid thermal reaction norms

   https://doi.org/10.1111/eva.12798  

   O'Donnell, Daniel R. ; Du, Zhi‐yan ; Litchman, Elena ( April 2019 , Evolutionary Applications)

   Temperature effects on the fatty acid (FA) profiles of phytoplankton, major primary producers in the ocean, have been widely studied due to their importance as industrial feedstocks and to their indispensable role as global producers of long‐chain, polyunsaturated FA (PUFA), including omega‐3 (ω3) FA required by organisms at higher trophic levels. The latter is of global ecological concern for marine food webs, as some evidence suggests an ongoing decline in global marine‐derived ω3 FA due to both a global decline in phytoplankton abundance and to a physiological reduction in ω3 production by phytoplankton as temperatures rise. Here, we examined both short‐term (physiological) and long‐term (evolutionary) responses of FA profiles to temperature by comparing FA thermal reaction norms of the marine diatomThalassiosira pseudonanaafter ~500 generations (ca. 2.5 years) of experimental evolution at low (16°C) and high (31°C) temperatures. We showed that thermal reaction norms for some key FA classes evolved rapidly in response to temperature selection, often in ways contrary to our predictions based on prior research. Notably, 31°C‐selected populations showed higher PUFA percentages (including ω3 FA) than 16°C‐selected populations at the highest assay temperature (31°C, aboveT. pseudonana'soptimum temperature for population growth), suggesting that high‐temperature selection led to an evolved ability to sustain high PUFA production at high temperatures. Rapid evolution may therefore mitigate some of the decline in global phytoplankton‐derived ω3 FA production predicted by recent studies. Beyond its implications for marine food webs, knowledge of the effects of temperature on fatty acid profiles is of fundamental importance to our understanding of the mechanistic causes and consequences of thermal adaptation.

    

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