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The colony-forming cyanobacteria Trichodesmium spp. are considered one of the most important nitrogen-fixing genera in the warm, low nutrient ocean. Despite this central biogeochemical role, many questions about their evolution, physiology, and trophic interactions remain unanswered. To address these questions, we describe Trichodesmium pangenomic potential via significantly improved genomic assemblies from two isolates and 15 new >50% complete Trichodesmium metagenome-assembled genomes from hand-picked, Trichodesmium colonies spanning the Atlantic Ocean. Phylogenomics identified ~four N2 fixing clades of Trichodesmium across the transect, with T. thiebautii dominating the colony-specific reads. Pangenomic analyses showed that all T. thiebautii MAGs are enriched in COG defense mechanisms and encode a vertically inherited Type III-B Clustered Regularly Interspaced Short Palindromic Repeats and associated protein-based immunity system (CRISPR-Cas). Surprisingly, this CRISPR-Cas system was absent in all T. erythraeum genomes, vertically inherited by T. thiebautii, and correlated with increased signatures of horizontal gene transfer. Additionally, the system was expressed in metaproteomic and transcriptomic datasets and CRISPR spacer sequences with 100% identical hits to field-assembled, putative phage genome fragments were identified. While the currently CO2-limited T. erythraeum is expected to be a ‘winner’ of anthropogenic climate change, their genomic dearth of known phage resistance mechanisms, compared to T. thiebautii, could put this outcome in question. Thus, the clear demarcation of T. thiebautii maintaining CRISPR-Cas systems, while T. erythraeum does not, identifies Trichodesmium as an ecologically important CRISPR-Cas model system, and highlights the need for more research on phage-Trichodesmium interactions.

 

In the surface waters of the warm oligotrophic ocean, filaments and aggregated colonies of the nitrogen (N)‐fixing cyanobacteriumTrichodesmiumcreate microscale nutrient‐rich oases. These hotspots fuel primary productivity and harbour a diverse consortium of heterotrophs. Interactions with associated microbiota can affect the physiology ofTrichodesmium, often in ways that have been predicted to support its growth. Recently, it was found that trimethylamine (TMA), a globally abundant organic N compound, inhibits N₂fixation in cultures ofTrichodesmiumwithout impairing growth rate, suggesting thatTrichodesmiumcan use TMA as an alternate N source. In this study,¹⁵N‐TMA DNA stable isotope probing (SIP) of aTrichodesmiumenrichment was employed to further investigate TMA metabolism and determine whether TMA‐N is incorporated directly or secondarily via cross‐feeding facilitated by microbial associates. Herein, we identify two members of the marineRoseobacterclade (MRC) of Alphaproteobacteria as the likely metabolizers of TMA and provide genomic evidence that they converted TMA into a more readily available form of N, e.g., ammonium (NH₄⁺), which was subsequently used byTrichodesmiumand the rest of the community. The results implicate microbiome‐mediated carbon (C) and N transformations in modulating N₂fixation and thus highlight the involvement of host‐associated heterotrophs in global biogeochemical cycling.

 

Throughout the open ocean, a minimum in dissolved iron concentration (dFe) overlaps with the deep chlorophyll maximum (DCM), which marks the lower limit of the euphotic zone. Maximizing light capture in these dim waters is expected to require upregulation of Fe-bearing photosystems, further depleting dFe and possibly leading to co-limitation by both iron and light. However, this effect has not been quantified for important phytoplankton groups like Prochlorococcus, which contributes most of the productivity in the oligotrophic DCM. Here, we present culture experiments with Prochlorococcus strain MIT1214, a member of the Low Light 1 ecotype isolated from the DCM in the North Pacific subtropical gyre. Under a matrix of iron and irradiance matching those found at the DCM, the ratio of Fe to carbon in Prochlorococcus MIT1214 cells ranged from 10–40 × 10−6 mol Fe:mol C and increased with light intensity and growth rate. These results challenge theoretical models predicting highest Fe:C at lowest light intensity, and are best explained by a large photosynthetic Fe demand that is not downregulated at higher light. To sustain primary production in the DCM with the rigid Fe requirements of low-light-adapted Prochlorococcus, dFe must be recycled rapidly and at high efficiency.

 

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.

 

A small subset of marine microbial enzymes and surface transporters have a disproportionately important influence on the cycling of carbon and nutrients in the global ocean. As a result, they largely determine marine biological productivity and have been the focus of considerable research attention from microbial oceanographers. Like all biological catalysts, the activity of these keystone biomolecules is subject to control by temperature and pH, leaving the crucial ecosystem functions they support potentially vulnerable to anthropogenic environmental change. We summarize and discuss both consensus and conflicting evidence on the effects of sea surface warming and ocean acidification for five of these critical enzymes [carbonic anhydrase, ribulose-1,5-bisphosphate carboxylase/oxygenase (RuBisCO), nitrogenase, nitrate reductase, and ammonia monooxygenase] and one important transporter (proteorhodopsin). Finally, we forecast how the responses of these few but essential biocatalysts to ongoing global change processes may ultimately help to shape the microbial communities and biogeochemical cycles of the future greenhouse ocean. 

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. 

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. 

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.