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1. Nutrient-Colimited Trichodesmium as a Nitrogen Source or Sink in a Future Ocean

   https://doi.org/10.1128/AEM.02137-17  

   Walworth, Nathan G. ; Fu, Fei-Xue ; Lee, Michael D. ; Cai, Xiaoni ; Saito, Mak A. ; Webb, Eric A. ; Hutchins, David A. ; Liu, Shuang-Jiang ( February 2018 , Applied and Environmental Microbiology)

   ABSTRACT Nitrogen-fixing (N 2 ) cyanobacteria provide bioavailable nitrogen to vast ocean regions but are in turn limited by iron (Fe) and/or phosphorus (P), which may force them to employ alternative nitrogen acquisition strategies. The adaptive responses of nitrogen fixers to global-change drivers under nutrient-limited conditions could profoundly alter the current ocean nitrogen and carbon cycles. Here, we show that the globally important N 2 fixer Trichodesmium fundamentally shifts nitrogen metabolism toward organic-nitrogen scavenging following long-term high-CO 2 adaptation under iron and/or phosphorus (co)limitation. Global shifts in transcripts and proteins under high-CO 2 /Fe-limited and/or P-limited conditions include decreases in the N 2 -fixing nitrogenase enzyme, coupled with major increases in enzymes that oxidize trimethylamine (TMA). TMA is an abundant, biogeochemically important organic nitrogen compound that supports rapid Trichodesmium growth while inhibiting N 2 fixation. In a future high-CO 2 ocean, this whole-cell energetic reallocation toward organic nitrogen scavenging and away from N 2 fixation may reduce new-nitrogen inputs by Trichodesmium while simultaneously depleting the scarce fixed-nitrogen supplies of nitrogen-limited open-ocean ecosystems. IMPORTANCE Trichodesmium is among the most biogeochemically significant microorganisms in the ocean, since it supplies up to 50% of the new nitrogen supporting open-ocean food webs. We usedmore »Trichodesmium cultures adapted to high-CO 2 conditions for 7 years, followed by additional exposure to iron and/or phosphorus (co)limitation. We show that “future ocean” conditions of high CO 2 and concurrent nutrient limitation(s) fundamentally shift nitrogen metabolism away from nitrogen fixation and instead toward upregulation of organic nitrogen-scavenging pathways. We show that the responses of Trichodesmium to projected future ocean conditions include decreases in the nitrogen-fixing nitrogenase enzymes coupled with major increases in enzymes that oxidize the abundant organic nitrogen source trimethylamine (TMA). Such a shift toward organic nitrogen uptake and away from nitrogen fixation may substantially reduce new-nitrogen inputs by Trichodesmium to the rest of the microbial community in the future high-CO 2 ocean, with potential global implications for ocean carbon and nitrogen cycling.« less
2. Modeling the physiology of the aquatic temnospondyl <i>Archegosaurusdecheni</i> from the early Permian of Germany

   https://doi.org/10.5194/fr-20-105-2017  

   Witzmann, Florian ; Brainerd, Elizabeth ( January 2017 , Fossil Record)

   Abstract. Physiological aspects like heat balance, gas exchange, osmoregulation, and digestion of the early Permian aquatic temnospondyl Archegosaurus decheni, which lived in a tropical freshwater lake, are assessed based on osteological correlates of physiologically relevant soft-tissue organs and by physiological estimations analogous to air-breathing fishes. Body mass (M) of an adult Archegosaurus with an overall body length of more than 1m is estimated as 7kg using graphic double integration. Standard metabolic rate (SMR) at 20°C (12kJh⁻¹) and active metabolic rate (AMR) at 25°C (47kJh⁻¹) were estimated according to the interspecific allometry of metabolic rate (measured as oxygen consumption) of all fish (V_O2 = 4. 8M^0. 88) and form the basis for most of the subsequent estimations. Archegosaurus is interpreted as a facultative air breather that got O₂ from the internal gills at rest in well-aerated water but relied on its lungs for O₂ uptake in times of activity and hypoxia. The bulk of CO₂ was always eliminated via the gills. Our estimations suggest that if Archegosaurus did not have gills and released 100% CO₂ from its lungs, it would have to breathe much more frequently to release enough CO₂ relative to the lung ventilation required formore »just O₂ uptake. Estimations of absorption and assimilation in the digestive tract of Archegosaurus suggest that an adult had to eat about six middle-sized specimens of the acanthodian fish Acanthodes (ca. 8cm body length) per day to meet its energy demands. Archegosaurus is regarded as an ammonotelic animal that excreted ammonia (NH₃) directly to the water through the gills and the skin, and these diffusional routes dominated nitrogen excretion by the kidneys as urine. Osmotic influx of water through the gills had to be compensated for by production of dilute, hypoosmotic urine by the kidneys. Whereas Archegosaurus has long been regarded as a salamander-like animal, there is evidence that its physiology was more fish- than tetrapod-like in many respects.

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3. Colony formation in <i>Phaeocystis antarctica</i>: connecting molecular mechanisms with iron biogeochemistry

   https://doi.org/10.5194/bg-15-4923-2018  

   Bender, Sara J. ; Moran, Dawn M. ; McIlvin, Matthew R. ; Zheng, Hong ; McCrow, John P. ; Badger, Jonathan ; DiTullio, Giacomo R. ; Allen, Andrew E. ; Saito, Mak A. ( January 2018 , Biogeosciences)

   Abstract. Phaeocystis antarctica is an important phytoplankter of the Ross Sea where it dominates the early season bloom after sea ice retreat and is a major contributor to carbon export. The factors that influence Phaeocystis colony formation and the resultant Ross Sea bloom initiation have been of great scientific interest, yet there is little known about the underlying mechanisms responsible for these phenomena. Here, we present laboratory and field studies on Phaeocystis antarctica grown under multiple iron conditions using a coupled proteomic and transcriptomic approach. P. antarctica had a lower iron limitation threshold than a Ross Sea diatom Chaetoceros sp., and at increased iron nutrition (&gt;120pM Fe') a shift from flagellate cells to a majority of colonial cells in P. antarctica was observed, implying a role for iron as a trigger for colony formation. Proteome analysis revealed an extensive and coordinated shift in proteome structure linked to iron availability and life cycle transitions with 327 and 436 proteins measured as significantly different between low and high iron in strains 1871 and 1374, respectively. The enzymes flavodoxin and plastocyanin that can functionally replace iron metalloenzymes were observed at low iron treatments consistent with cellular iron-sparing strategies, with plastocyanin havingmore »a larger dynamic range. The numerous isoforms of the putative iron-starvation-induced protein (ISIP) group (ISIP2A and ISIP3) had abundance patterns coinciding with that of either low or high iron (and coincident flagellate or the colonial cell types in strain 1871), implying that there may be specific iron acquisition systems for each life cycle type. The proteome analysis also revealed numerous structural proteins associated with each cell type: within flagellate cells actin and tubulin from flagella and haptonema structures as well as a suite of calcium-binding proteins with EF domains were observed. In the colony-dominated samples a variety of structural proteins were observed that are also often found in multicellular organisms including spondins, lectins, fibrillins, and glycoproteins with von Willebrand domains. A large number of proteins of unknown function were identified that became abundant at either high or low iron availability. These results were compared to the first metaproteomic analysis of a Ross Sea Phaeocystis bloom to connect the mechanistic information to the in situ ecology and biogeochemistry. Proteins associated with both flagellate and colonial cells were observed in the bloom sample consistent with the need for both cell types within a growing bloom. Bacterial iron storage and B₁₂ biosynthesis proteins were also observed consistent with chemical synergies within the colony microbiome to cope with the biogeochemical conditions. Together these responses reveal a complex, highly coordinated effort by P. antarctica to regulate its phenotype at the molecular level in response to iron and provide a window into the biology, ecology, and biogeochemistry of this group.

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4. Diazotrophic <i>Trichodesmium</i> impact on UV–Vis radiance and pigment composition in the western tropical South Pacific

   https://doi.org/10.5194/bg-15-5249-2018  

   Dupouy, Cécile ; Frouin, Robert ; Tedetti, Marc ; Maillard, Morgane ; Rodier, Martine ; Lombard, Fabien ; Guidi, Lionel ; Picheral, Marc ; Neveux, Jacques ; Duhamel, Solange ; et al ( January 2018 , Biogeosciences)

   Abstract. We assessed the influence of the marine diazotrophic cyanobacterium Trichodesmium on the bio-optical properties of western tropical South Pacific (WTSP) waters (18–22°S, 160°E–160°W) during the February–March 2015 OUTPACE cruise. We performed measurements of backscattering and absorption coefficients, irradiance, and radiance in the euphotic zone with a Satlantic MicroPro free-fall profiler and took Underwater Vision Profiler 5 (UPV5) pictures for counting the largest Trichodesmium spp. colonies. Pigment concentrations were determined by fluorimetry and high-performance liquid chromatography and picoplankton abundance by flow cytometry. Trichome concentration was estimated from pigment algorithms and validated by surface visual counts. The abundance of large colonies counted by the UVP5 (maximum 7093coloniesm⁻³) was well correlated to the trichome concentrations (maximum 2093trichomesL⁻¹) with an aggregation factor of 600. In the Melanesian archipelago, a maximum of 4715trichomesL⁻¹ was enumerated in pump samples (3.2m) at 20°S,16730°E. High Trichodesmium abundance was always associated with absorption peaks of mycosporine-like amino acids (330, 360nm) and high particulate backscattering, but not with high Chl a fluorescence or blue particulate absorption (440nm). Along the west-to-east transect, Trichodesmium together with Prochlorococcus represented the major part of total chlorophyll concentration; themore »contribution of other groups were relatively small or negligible. The Trichodesmium contribution to total chlorophyll concentration was the highest in the Melanesian archipelago around New Caledonia and Vanuatu (60%), progressively decreased to the vicinity of the islands of Fiji (30%), and reached a minimum in the South Pacific Gyre where Prochlorococcus dominated chlorophyll concentration. The contribution of Trichodesmium to zeaxanthin was respectively 50, 40 and 20% for these regions. During the OUTPACE cruise, the relationship between normalized water-leaving radiance (nL_w) in the ultraviolet and visible and chlorophyll concentration was similar to that found during the BIOSOPE cruise in the eastern tropical Pacific. Principal component analysis (PCA) of OUTPACE data showed that nL_w at 305, 325, 340, 380, 412 and 440nm was strongly correlated to chlorophyll and zeaxanthin, while nL_w at 490 and 565nm exhibited lower correlations. These results, as well as differences in the PCA of BIOSOPE data, indicated that nL_w variability in the greenish blue and yellowish green during OUTPACE was influenced by other variables associated with Trichodesmium presence, such as backscattering coefficient, phycoerythrin fluorescence and/or zeaxanthin absorption, suggesting that Trichodesmium detection should involve examination of nL_w in this spectral domain.

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5. Mechanisms and heterogeneity of in situ mineral processing by the marine nitrogen fixer Trichodesmium revealed by single-colony metaproteomics

   https://doi.org/10.1038/s43705-021-00034-y  

   Held, Noelle A. ; Sutherland, Kevin M. ; Webb, Eric A. ; McIlvin, Matthew R. ; Cohen, Natalie R. ; Devaux, Alexander J. ; Hutchins, David A. ; Waterbury, John B. ; Hansel, Colleen M. ; Saito, Mak A. ( July 2021 , ISME Communications)

   The keystone marine nitrogen fixerTrichodesmiumthrives in high-dust environments. While laboratory investigations have observed thatTrichodesmiumcolonies can access the essential nutrient iron from dust particles, less clear are the biochemical strategies underlying particle–colony interactions in nature. Here we demonstrate thatTrichodesmiumcolonies engage with mineral particles in the wild with distinct molecular responses. We encountered particle-ladenTrichodesmiumcolonies at a sampling location in the Southern Caribbean Sea; microscopy and synchrotron-based imaging then demonstrated heterogeneous associations with iron oxide and iron-silicate minerals. Metaproteomic analysis of individual colonies by a new low-biomass approach revealed responses in biogeochemically relevant proteins including photosynthesis proteins and metalloproteins containing iron, nickel, copper, and zinc. The iron-storage protein ferritin was particularly enriched implying accumulation of mineral-derived iron, and multiple iron acquisition pathways including Fe(II), Fe(III), and Fe-siderophore transporters were engaged. While the particles provided key trace metals such as iron and nickel, there was also evidence thatTrichodesmiumwas altering its strategy to confront increased superoxide production and metal exposure. Chemotaxis regulators also responded to mineral presence suggesting involvement in particle entrainment. These molecular responses are fundamental toTrichodesmium’secological success and global biogeochemical impact, and may contribute to the leaching of particulate trace metals with implications for global iron and carbon cycling.