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Nitrogen fixation in the widely distributed marine gammaproteobacteria diazotroph Candidatus Thalassolituus haligoni

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Abstract

The high diversity and global distribution of heterotrophic bacterial diazotrophs (HBDs) in the ocean has recently become apparent. However, understanding the role these largely uncultured microorganisms play in marine N2 fixation poses a challenge due to their undefined growth requirements and the complex regulation of the nitrogenase enzyme. We isolated and characterized Candidatus Thalassolituus haligoni, a member of a widely distributed clade of HBD belonging to the Oceanospirillales. Analysis of its nifH gene via amplicon sequencing revealed the extensive distribution of Cand. T. haligoni across the Pacific, Atlantic, and Arctic Oceans. Pangenome analysis indicates that the isolate shares >99% identity with an uncultured metagenome-assembled genome called Arc-Gamma-03, recently recovered from the Arctic Ocean. Through combined genomic, proteomic, and physiological approaches, we confirmed that the isolate fixes N2 gas. However, the mechanisms governing nitrogenase regulation in Cand. T. haligoni remain unclear. We propose Cand. T. haligoni as a globally distributed, cultured HBD model species within this understudied clade of Oceanospirillales.

Figure

Fig. 1. Scanning electron microscopy and genomic, proteomic, and genome-assisted metabolic models of Cand. T. haligoni.
(A) (A) cell morphology of the isolate under n2- fixing conditions using scanning electron microscopy (SeM; top) and transmission electron microscopy (teM; bottom). SeM magnification = 17.71 × 103. Arrows indicate flagella (F) and PhB granules (PhB).
(B) CProteome-genome circular map under nO3− depleted conditions. Starting from the innermost ring: Gc content (gray), Gc skew for forward (green) and reverse strands (magenta), leading and lagging strand cdSs (light purple), and detected proteins (blue). Arrows in the genome indicate genes of interest [nif clusters, n2 fixation–related genes are molybdate uptake and transformation genes (mod factors), tRAP-c4 uptake, and glutamine synthesis] and have corresponding detected proteins highlighted in respective colors. White spaces in the proteome indicate regions not detected.
(C) Nif clusters (red, blue, and orange) and associated n2 fixation genes (gray). n2 fixation–associated genes include glycogen phosphorylase and glycogen uptake genes. numbers along the line indicate base-pair locations within the genome. A nucleotide break in the center of the diagram from 3,598,007 nt to 3,737,467 nt is represented by the zig-zag line in red (concatenated). Clusters are color-coded to the associated nif clusters, with accessory genes to that cluster indicated by respective color hues.
(D) Simplified metabolic schematic of the isolate based on the genome annotation. the schematic was created using the RASt server and BioRender.

 

Reference

Sonja A. Rose, Brent M. Robicheau, Jennifer Tolman, Debany Fonseca-Batista, Elden Rowland, Dhwani Desai, Jenni-Marie Ratten, Ella Joy H. Kantor, André M. Comeau, Morgan G.I. Langille, Jon Jerlström-Hultqvist, Emmanuel Devred, Géraldine Sarthou, Erin M. Bertrand and Julie La Roche. “Nitrogen fixation in the widely distributed marine γ-proteobacterial diazotroph Candidatus Thalassolituus haligoni“. Science Advances Volume 10, Issue 31 (Aug 2024)

https://www.science.org/doi/epdf/10.1126/sciadv.adn1476

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A CO₂ sink in the South Pacific marine desert

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Four colleagues from LEMAR (Jérémie Habasque, Frédéric Le Moigne, Anne Lebourges-Dhaussy et Géraldine Sarthou) have participated in a major international study based on the results of the TONGA cruise. This study, led by Sophie Bonnet (MIO) and Cécile Guieu (LOV) focuses on the mechanism of natural iron fertilisation in the ocean by hydrothermal springs, and has just been published in the prestigious journal Science.

Press release

A newly identified process of natural iron fertilisation in the ocean feeds regional CO₂ sinks. This is shown by a study published on 25 May in Science and co-authored by 25 researchers from the Tonga project led by two researchers from IRD and CNRS, bringing together more than 90 scientists from 14 French laboratories based in mainland France and New Caledonia, and 6 international universities. In this article, the research team studied the shallow submarine volcanoes of the Tonga volcanic arc (South Pacific), which release hydrothermal fluids rich in iron, a micronutrient essential for life. Some of the iron emitted in these fluids reaches the lighted layer of the ocean, where photosynthesis takes place, i.e. the fixation of CO₂ by the microalgae of the plankton. This strongly stimulates biological activity in this zone, particularly that of diazotrophs1, creating a vast bloom of around 400,000 km2, a veritable oasis of life in the middle of the South Pacific marine desert, and increased sequestration of CO2 towards the deep ocean.

To document the mechanistic link between the supply of iron by submarine volcanism and the response of the surface plankton community, the researchers combined acoustic, chemical, physical and biological observations acquired during the Tonga oceanographic expedition, to be carried out in 2019 on board the L’Atalante vessel of the French Oceanographic Fleet operated by Ifremer.

 

In this study, scientists demonstrate that the fluids emitted along Tonga’s volcanic arc have a considerable impact on iron concentrations in the illuminated layer. This enrichment stimulates biological activity, leading to the formation of a vast oasis of chlorophyll-rich life, dominated by the diazotroph Trichodesmium. Compared with adjacent waters not fertilised with iron, diazotroph activity is 2 to 8 times higher and carbon sequestration fluxes in the deep ocean 2 to 3 times. These results reveal a mechanism of natural iron fertilisation in the ocean by hydrothermal springs, which feeds regional atmospheric CO2 sinks.

Planktonic diazotrophs are microscopic organisms that are ubiquitous in the ocean. They play a crucial role, acting as natural fertilisers by providing newly available nitrogen to the surface ocean biosphere, an essential nutrient that is in short supply in most of our oceans. The western subtropical South Pacific is a hotbed of diazotroph activity, contributing an estimated 21% of the world’s nitrogen through this process.

The input of iron via atmospheric deposition is known to control the biogeography of diazotrophs on a large scale, but these aeolian inputs are extremely low in this remote region. This suggests the presence of other iron fertilisation processes, such as the one highlighted here for the first time. Identifying these processes is of the utmost importance as diazotrophs have recently been identified as key drivers of future CO2 fixation by the ocean in response to climate change.

 

 

Reference
Sophie Bonnet, Cécile Guieu, Vincent Taillandier, Cédric Boulart, Pascale Bouruet-Aubertot, Frédéric Gazeau, Carla Scalabrin, Matthieu Bressac, Angela N. Knapp, Yannis Cuypers, David González-Santana, Heather J. Forrer, Jean-Michel Grisoni, Olivier Grosso, Jérémie Habasque, Mercedes Jardin-Camps, Nathalie Leblond, Frédéric Le Moigne, Anne Lebourges-Dhaussy, Caroline Lory, Sandra Nunige, Elvira Pulido-Villena, Andrea L. Rizzo, Géraldine Sarthou, Chloé Tilliette.
Institut méditerranéen d’océanologie (CNRS/Aix-Marseille Université/IRD/Université de Toulon), Laboratoire d’océanographie de Villefranche (CNRS/Sorbonne Université), Laboratoire Adaptation et diversité en milieu marin (CNRS/SU), Laboratoire d’océanographie et du climat : expérimentations et approches numériques (CNRS/IRD/MNHN/SU), Laboratoire Geo-ocean (CNRS/Ifremer/UBO), Laboratoire des sciences de l’environnement marin (CNRS/IRD/Ifremer/UBO), Institut de la Mer de Villefranche (CNRS/SU).
Natural iron fertilization by shallow hydrothermal sources fuels diazotroph blooms in the Ocean, Science, 25 mai 2023. DOI: 10.1126/science.abq4654.

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Radiolarians and the silicon cycle: Natalia Llopis-Monferrer’s work in the spotlight!

The American Geophysical Union (AGU) has declared “Research Spotlight” the recent article by Natalia Llopis-Monferrer in “Global Biogeochemical Cycles” on the importance of radiolarians (marine planktonic organisms) in the silicon cycle of the world ocean.

This recent work re-evaluates the role of these tiny protists, which could contribute up to one-fifth of the world’s silica production by marine organisms.

Natalia Llopis-Monferer is a spanish student at LEMAR (UMR 6539). She is co-supervised by Aude Leynaert (CNRS), Fabrice Not (SBR) and Paul Tréguer (UBO).

Read the “EOS” article (Sciences News by AGU)

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Sponge skeletons as an important sink of silicon in the global oceans

Silicon (Si) is a pivotal element in the biogeochemical and ecological functioning of the ocean. The marine Si cycle is thought to be in internal equilibrium, but the recent discovery of Si entries through groundwater and glacial melting have increased the known Si inputs relative to the outputs in the global oceans. Known outputs are due to the burying of diatom skeletons or their conversion into authigenic clay by reverse weathering. Here we show that non-phototrophic organisms, such as sponges and radiolarians, also facilitate significant Si burial through their siliceous skeletons. Microscopic examination and digestion of sediments revealed that most burial occurs through sponge skeletons, which, being unusually resistant to dissolution, had passed unnoticed in the biogeochemical inventories of sediments. The preservation of sponge spicules in sediments was 45.2 ± 27.4%, but only 6.8 ± 10.1% for radiolarian testa and 8% for diatom frustules. Sponges lead to a global burial flux of 1.71 ± 1.61 TmolSi yr−1 and only 0.09 ± 0.05 TmolSi yr−1 occurs through radiolarians. Collectively, these two non-phototrophically produced silicas increase the Si output of the ocean to 12.8 TmolSi yr−1, which accounts for a previously ignored sink that is necessary to adequately assess the global balance of the marine Si cycle.

References

Maldonado, M., López-Acosta, M., Sitjà, C., García-Puig, M., Galobart, C., Ercilla, G., & Leynaert, A. (2019). Sponge skeletons as an important sink of silicon in the global oceans. Nature Geoscience. https://doi.org/10.1038/s41561-019-0430-7

 

Read the publication

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Daniel Conley’s seminar (Lund University, Sweden) on April 29

On April 29th at 10am in room A215 (IUEM) we will welcome Daniel Conley from Lund University in Sweden who will present his work on the following theme:

Constraining variations in the global biogeochemical silica cycle through geologic time.

Summary of his presentation:

It is widely recognized that the emergence and expansion of silica biomineralization in the oceans has affected evolutionary competition for dissolved Si (DSi). This resulted in changes in the global biogeochemical cycles of silica, carbon (C) and other nutrients that regulate ocean productivity and ultimately climate. However, a series of very recent discoveries in geology and biology suggest that the first biological impacts on the global Si cycle were likely by prokaryotes during the Archean with further decreases in oceanic DSi with the evolution of widespread, large-scale skeletal biosilicification significantly earlier than the current paradigm. Our project interweaves geology and biology and will create new knowledge into the interactions between biosilicification in organisms and the environment and how these interactions have evolved through Earth’s history. Together, these geological and biological analyses will provide novel insights into the key events during periods of DSi drawdown, which reorganize the distribution of carbon and nutrients, changing energy flow and productivity in the biological communities of the ancient oceans.

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Tag Archive for: biogeochemical cycle

Glass

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BaSIS

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RadiCal

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Tag Archive for: biogeochemical cycle

Lucie CASSARINO

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