Phytoplankton surveys in the Arctic Fram Strait demonstrate the tiny eukaryotic alga Micromonas and other picoprasinophytes contribute to deep sea export

© The Author(s), 2022. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Bachy, C., Sudek, L., Choi, C. J., Eckmann, C. A., Nöthig, E.-M., Metfies, K., & Worden, A. Z. Phytoplankton surveys in the Arctic Fram Strait demonstrate the tiny eukaryotic alga Micromonas and other picoprasinophytes contribute to deep sea export. Microorganisms, 10(5), (2022): 961, https://doi.org/10.3390/microorganisms10050961.Critical questions exist regarding the abundance and, especially, the export of picophytoplankton (≤2 µm diameter) in the Arctic. These organisms can dominate chlorophyll concentrations in Arctic regions, which are subject to rapid change. The picoeukaryotic prasinophyte Micromonas grows in polar environments and appears to constitute a large, but variable, proportion of the phytoplankton in these waters. Here, we analyze 81 samples from the upper 100 m of the water column from the Fram Strait collected over multiple years (2009–2015). We also analyze sediment trap samples to examine picophytoplankton contributions to export, using both 18S rRNA gene qPCR and V1-V2 16S rRNA Illumina amplicon sequencing to assess the Micromonas abundance within the broader diversity of photosynthetic eukaryotes based on the phylogenetic placement of plastid-derived 16S amplicons. The material sequenced from the sediment traps in July and September 2010 showed that 11.2 ± 12.4% of plastid-derived amplicons are from picoplanktonic prasinophyte algae and other green lineage (Viridiplantae) members. In the traps, Micromonas dominated (83.6 ± 21.3%) in terms of the overall relative abundance of Viridiplantae amplicons, specifically the species Micromonas polaris. Temporal variations in Micromonas abundances quantified by qPCR were also observed, with higher abundances in the late-July traps and deeper traps. In the photic zone samples, four prasinophyte classes were detected in the amplicon data, with Micromonas again being the dominant prasinophyte, based on the relative abundance (89.4 ± 8.0%), but with two species (M. polaris and M. commoda-like) present. The quantitative PCR assessments showed that the photic zone samples with higher Micromonas abundances (>1000 gene copies per mL) had significantly lower standing stocks of phosphate and nitrate, and a shallower average depth (20 m) than those with fewer Micromonas. This study shows that despite their size, prasinophyte picophytoplankton are exported to the deep sea, and that Micromonas is particularly important within this size fraction in Arctic marine ecosystems.This research was supported by funding from the National Science Foundation (NSF) DEB-1639033, Gordon and Betty Moore Foundation Marine Investigator Award grant 3788, and fellowships from the Radcliffe Institute for Advanced Research at Harvard University and the Hanse-Wissenschaftskolleg for Marine and Climate Science, awarded to A.Z.W. Contribution to HGF POF-IV 6.1, 6.3, and 6.4

Submarine Basaltic Glass Colonization by the Heterotrophic Fe(II)-Oxidizing and Siderophore-Producing Deep-Sea Bacterium

Phylogenetically and metabolically diverse bacterial communities have been found in association with submarine basaltic glass surfaces. The driving forces behind basalt colonization are for the most part unknown. It remains ambiguous if basalt provides ecological advantages beyond representing a substrate for surface colonization, such as supplying nutrients and/or energy. Pseudomonas stutzeri VS-10, a metabolically versatile bacterium isolated from Vailulu'u Seamount, was used as a model organism to investigate the physiological responses observed when biofilms are established on basaltic glasses. In Fe-limited heterotrophic media, P. stutzeri VS-10 exhibited elevated growth in the presence of basaltic glass. Diffusion chamber experiments demonstrated that physical attachment or contact of soluble metabolites such as siderophores with the basaltic glass plays a pivotal role in this process. Electrochemical data indicated that P. stutzeri VS-10 is able to use solid substrates (electrodes) as terminal electron donors and acceptors. Siderophore production and heterotrophic Fe(II) oxidation are discussed as potential mechanisms enhancing growth of P. stutzeri VS-10 on glass surfaces. In correlation with that we discuss the possibility that metabolic versatility could represent a common and beneficial physiological trait in marine microbial communities being subject to oligotrophic and rapidly changing deep-sea conditions

Publisher Correction: Genetic tool development in marine protists: emerging model organisms for experimental cell biology.

An amendment to this paper has been published and can be accessed via a link at the top of the paper

Genetic tool development in marine protists: emerging model organisms for experimental cell biology

Abstract: Diverse microbial ecosystems underpin life in the sea. Among these microbes are many unicellular eukaryotes that span the diversity of the eukaryotic tree of life. However, genetic tractability has been limited to a few species, which do not represent eukaryotic diversity or environmentally relevant taxa. Here, we report on the development of genetic tools in a range of protists primarily from marine environments. We present evidence for foreign DNA delivery and expression in 13 species never before transformed and for advancement of tools for eight other species, as well as potential reasons for why transformation of yet another 17 species tested was not achieved. Our resource in genetic manipulation will provide insights into the ancestral eukaryotic lifeforms, general eukaryote cell biology, protein diversification and the evolution of cellular pathways

Genetic tool development in marine protists: emerging model organisms for experimental cell biology

Abstract: Diverse microbial ecosystems underpin life in the sea. Among these microbes are many unicellular eukaryotes that span the diversity of the eukaryotic tree of life. However, genetic tractability has been limited to a few species, which do not represent eukaryotic diversity or environmentally relevant taxa. Here, we report on the development of genetic tools in a range of protists primarily from marine environments. We present evidence for foreign DNA delivery and expression in 13 species never before transformed and for advancement of tools for eight other species, as well as potential reasons for why transformation of yet another 17 species tested was not achieved. Our resource in genetic manipulation will provide insights into the ancestral eukaryotic lifeforms, general eukaryote cell biology, protein diversification and the evolution of cellular pathways

Ecology of microbe/basaltic glass interactions : mechanisms and diversity

Submarine basaltic glass constitutes a major part of the oceanic crust and contains a number of bio-essential nutrients including Fe and Mn. Substantial biological activity can be inferred from bio-alteration textures that dominate basaltic glass alteration. However, the role of basaltic glass in fueling diverse chemolithotrophic communities within deep-sea ecosystems remains enigmatic. Little is known about the key mechanisms and potential ecological advantages that drive basaltic glass colonization, the extent to which microbial activity may affect alteration rates and the biogeochemical cycling of elements in particular along the basalt/water interface. The nutrient and energy availability in basalt is considered to facilitate these processes. Seamounts are substantial outcrops of the oceanic lithosphere and offer natural laboratories for the study the ecology of microbe/ basaltic glass interactions. Studies of natural rock surfaces and hydrothermal metal-oxy-hydroxides from different hydrothermal settings at Vailulu'u Seamount (American Samoa), resulted in a detailed characterization of microbial communities and the isolation of a large number of metabolically diverse microbes. One of these strains, Pseudomonas stutzeri VS-10, was chosen as a model organism to study the processes of microbe/basaltic glass interactions. It was isolated from a rhyolite microbial trap and exhibits elevated growth under nutrient limited conditions in the presence of basalt. Key metabolic traits of VS-10 include heterotrophic Fe (II)-oxidation and siderophore production. I investigated this strain with respect to a number of metabolic processes, including the oxidative transformation of Fe and Mn, the production of metabolic byproducts (e.g. organic acids) and secondary metabolites (siderophores) along with their effects on the bio-alteration of the glass. Methods employed include Scanning Electron and Atomic Force Microscopy (SEM and AFM), Inductively Coupled Plasma Optical Emission Spectroscopy (ICP-OES), Reversed-phase High Performance Liquid Chromatography (HPLC), Liquid Chromatography Electrospray Ionization Mass Spectrometry (LC-ESI-MS) and microbial fuel cells (MFC). Fe availability and direct contact of the bacterium with the rock surface was shown to significantly facilitate growth of the strain suggesting basaltic glass as an important substratum in supporting metabolically diverse microbial communities in deep-sea ecosystem

Reactions of a Chromium(III)-Superoxo Complex and Nitric Oxide That Lead to the Formation of Chromium(IV)-Oxo and Chromium(III)-Nitrito Complexes

The reaction of an end-on Cr­(III)-superoxo complex bearing a 14-membered tetraazamacrocyclic TMC ligand, [Cr^III(14-TMC)­(O₂)­(Cl)]⁺, with nitric oxide (NO) resulted in the generation of a stable Cr­(IV)-oxo species, [Cr^IV(14-TMC)­(O)­(Cl)]⁺, via the formation of a Cr­(III)-peroxynitrite intermediate and homolytic O–O bond cleavage of the peroxynitrite ligand. Evidence for the latter comes from electron paramagnetic resonance spectroscopy, computational chemistry and the observation of phenol nitration chemistry. The Cr­(IV)-oxo complex does not react with nitrogen dioxide (NO₂), but reacts with NO to afford a Cr­(III)-nitrito complex, [Cr^III(14-TMC)­(NO₂)­(Cl)]⁺. The Cr­(IV)-oxo and Cr­(III)-nitrito complexes were also characterized spectroscopically and/or structurally

Intron Invasions Trace Algal Speciation and Reveal Nearly Identical Arctic and Antarctic Micromonas Populations.

Spliceosomal introns are a hallmark of eukaryotic genes that are hypothesized to play important roles in genome evolution but have poorly understood origins. Although most introns lack sequence homology to each other, new families of spliceosomal introns that are repeated hundreds of times in individual genomes have recently been discovered in a few organisms. The prevalence and conservation of these introner elements (IEs) or introner-like elements in other taxa, as well as their evolutionary relationships to regular spliceosomal introns, are still unknown. Here, we systematically investigate introns in the widespread marine green alga Micromonas and report new families of IEs, numerous intron presence-absence polymorphisms, and potential intron insertion hot-spots. The new families enabled identification of conserved IE secondary structure features and establishment of a novel general model for repetitive intron proliferation across genomes. Despite shared secondary structure, the IE families from each Micromonas lineage bear no obvious sequence similarity to those in the other lineages, suggesting that their appearance is intimately linked with the process of speciation. Two of the new IE families come from an Arctic culture (Micromonas Clade E2) isolated from a polar region where abundance of this alga is increasing due to climate induced changes. The same two families were detected in metagenomic data from Antarctica--a system where Micromonas has never before been reported. Strikingly high identity between the Arctic isolate and Antarctic coding sequences that flank the IEs suggests connectivity between populations in the two polar systems that we postulate occurs through deep-sea currents. Recovery of Clade E2 sequences in North Atlantic Deep Waters beneath the Gulf Stream supports this hypothesis. Our research illuminates the dynamic relationships between an unusual class of repetitive introns, genome evolution, speciation, and global distribution of this sentinel marine alga