The IRON cycle in deep-sea hydrothermal vents: role of iron-reducing and iron-oxidizing MIcroorganisms and impact on MInerals alteration – IRON2MI
The IRON cycle in deep-sea hydrothermal vents: contribution of iron-reducing and iron-oxidizing MIcroorganisms and impact on MInerals alteration (IRON2MI)
We address 3 main hypotheses: (i) the characterization of new taxa involved in Fe-cycle, in addition to those already known, and the study of their metabolic pathways will allow to identify new Fe gene markers, (ii) the use of Fe gene markers will allow to study the structure and functions of microbial communities involved in the Fe cycle at the scale of a hydrothermal site, and (iii) microorganisms using Fe in their energy pathways contribute significantly to the alteration of Fe-rich minerals.
Context and main objective of the IRON2MI project
In front of the increasing societal demand for deep-sea mining and the future quantification and exploitation of the deep-sea mineral resources, it is of importance to better understand the contribution of the microbial compartment on the mineral alteration processes that can participate to the modification of the nature of mineral resources (Boschen et al., 2013). Deep-sea hydrothermal vent sites are characterized by hard seafloor massive sulfide (SMS) deposits enriched with a high content of base metals (zinc, iron (Fe), lead, and copper), sulfides and rare elements, such as gold, silver, cobalt, and indium. Since several decades, these SMS deposits are attractive to mining companies and industrialized countries that are encouraged by the increasing demand for mineral raw materials due to constant population growth, rising living standards, urbanization, technological advance, and, more recently, the transition to a low-carbon economy (Boschen et al., 2013; Murton et al., 2019). Despite the significant scientific resources deployed to study these deep-sea ecosystems (diversity and functions), considerable efforts are needed to better characterize them and to anticipate the impact of future mining exploitations. Among metals present in SMS deposits at deep-sea hydrothermal sites, Fe is found at significant concentrations in sulfide minerals and be under a solid form such as pyrite, chalcopyrite, marcasite or pyrrhotite or to be in complexed minerals such as iron oxyhydroxides (Haymon, 1983; Toner et al., 2009). These Fe-rich minerals are involved in the energy metabolism of, still relatively unexplored microbial communities, as electron donor (Fe2+) or acceptor (Fe3+) leading to their alteration/mineralization (Edwards et al., 2003; Emerson et al., 2007 ; Slobodkina et al., 2009a; Singer et al., 2011; Makita et al., 2017; Chen et al., 2021). It is important to consider that, alteration processes are defined by all modifications of the physico-chemical properties of minerals by biotic or abiotic reactions, whereas mineralization processes involve the precipitation of elements (from a liquid or solid phase) by biotic or abiotic reactions in order to participate in the formation of mineral surfaces. The main objective of the IRON2MI project is to characterize Fe3+-reducing and Fe2+-oxidizing microorganisms by studying their physiology and metabolic pathways, and by assessing the structure of these microbial communities and their role in the alteration/mineralization of Fe-rich minerals, especially in the context of the future exploitation of hydrothermal polymetallic sulfide mining resources.
• WP1 Physiology and metabolic pathways of novel Fe-reducing and Fe-oxidizing microorganisms isolated from deep-sea hydrothermal vents To gain a better knowledge of the microbial actors involved in Fe cycle in deep-sea hydrothermal vent ecosystems, the IRON2MI project will benefit from fresh samples that were collected during the HERMINE2 (summer 2022) and BICOSE3 (winter 2023) oceanographic cruises at the Mid-Atlantic Ridge (MAR; depth of 3600 m; TAG and Snake Pit fields). Based on these samples, the aims of this WP are i) to isolate and characterize up to three new strains for each process (Fe-reduction and Fe-oxidation) and then to study their ecophysiological properties, their genomes and their morphology, ii) to investigate more deeply the metabolic pathways of Fe-reduction and oxidation compared to what is known, by combining complementary approaches such as comparative genomics, transcriptomics and by monitoring substrates, intermediates and end metabolic products, and iii) according to the metabolic pathways obtained, new genetic markers for both Fe-reduction and oxidation will be defined.
• WP2 Structure and functions of in situ microbial communities involved in Fe cycle at the scale of a deep-sea hydrothermal site To carry out this WP, a sampling strategy consisting of sampling along a transect from the hot area to the cold area of a hydrothermal vent site will be carried out during the HERMINE2 or BICOSE3 cruises. From these samples, the structure and functions of microbial communities involved in Fe cycle will be studied by metabarcoding and metagenomic analyses using marker genes designed in WP1 and/or existing marker genes (mtrAB (reduction) or Cyc2 (oxidation) gene markers). Shipboard measurements (BICOSE3 cruise) of autotrophic and heterotrophic activity will also be carried out with and without supplementation with Fe2+ and Fe3+. In addition, microbial assemblages will be visualized using imagery techniques to better understand the spatial organization of these communities as well as the possible interactions between microorganisms and their substrate.
• WP3 Experimental quantification of the biotic alteration of Fe-rich minerals The alteration of Fe-rich minerals will be evaluated in vitro, with gas-lift bioreactors using natural microbial communities, by monitoring microbial growth and mineral alteration. Geochemical analyses will be carried out by a collaborator with strong geochemical expertise, in an attempt to quantify the weathering products of Fe-rich minerals due to biotic Fe-oxidation or reduction. To achieve this, approaches such as X-ray absorption spectroscopy, X-ray diffraction, SEM, Fe isotopic analyses and geochemical analyses of major and trace elements will be implemented. In parallel, microbial communities will be described by metabarcoding and/or meta-transcriptomic to cross link geochemistry data and the structure and functions of microbial communities during biotic alteration of Fe-rich minerals.
Main expected results: - The characterization of up to 3 new microbial strains for each process (Fe3+-reduction and Fe2+-oxidation). - The identification of new genetic markers for both Fe3+-reduction and Fe2+-oxidation processes. - The characterization of in situ microbial communities (taxonomic and functional diversity) involved in the Fe-cycle at the scale of a deep-sea hydrothermal vent. - Characterization of the role of Fe3+-reducing and Fe2+-oxidizing microorganisms in the alteration/mineralization of Fe-rich minerals.
The IRON2MI project focuses on the two main microbial processes of the Fe cycle in order to get a global view of this cycle in deep-sea hydrothermal vent ecosystems. By combining microbiological and geochemical investigations, the project will improve our knowledge of the diversity, structure and functions of microbial communities involved in the Fe cycle. Furthermore, in view of the increasing societal demand for mineral resources and future oceanic mining projects targeting polymetallic sulfide deposits, it is important to determine the contribution of microbial communities involved in the alteration of Fe-rich minerals. This latter aspect is significant to understand the impact of deep-sea mining and the evolution of sulfides seafloor deposits.
References:
Boschen, R. E., Rowden, A. A., Clark, M. R., & Gardner, J. P. (2013). Mining of deep-sea seafloor massive sulfides: a review of the deposits, their benthic communities, impacts from mining, regulatory frameworks and management strategies. Ocean Coast. Manag., 84, 54-67.
Chen, Y., He, Y., Shao, Z., Han, X., Chen, D., Yang, J., & Zeng, X. (2021). Thermosipho ferrireducens sp. nov., an anaerobic thermophilic iron (III)-reducing bacterium isolated from a deep-sea hydrothermal sulfide deposits. Int. J. Syst. Evol. Microbiol., 71(7), 004929.
Edwards, K. J., McCollom, T. M., Konishi, H., & Buseck, P. R. (2003). Seafloor bioalteration of sulfide minerals: results from in situ incubation studies. Geoch. Cosmochim. Acta, 67(15), 2843-2856.
Emerson, D., Rentz, J. A., Lilburn, T. G., Davis, R. E., Aldrich, H., Chan, C., & Moyer, C. L. (2007). A novel lineage of proteobacteria involved in formation of marine Fe-oxidizing microbial mat communities. PloS one, 2(8), e667.
Haymon, R. M. (1983). Growth history of hydrothermal black smoker chimneys. Nature, 301(5902), 695-698.
Makita, H., Tanaka, E., Mitsunobu, S., Miyazaki, M., Nunoura, T., Uematsu, K., ... & Takai, K. (2017). Mariprofundus micogutta sp. nov., a novel iron-oxidizing zetaproteobacterium isolated from a deep-sea hydrothermal field at the Bayonnaise knoll of the Izu-Ogasawara arc, and a description of Mariprofundales ord. nov. and Zetaproteobacteria classis nov. Arch. Microbiol., 199(2), 335-346.
Murton, B. J., Lehrmann, B., Dutrieux, A. M., Martins, S., de la Iglesia, A. G., Stobbs, I. J., ... & Petersen, S. (2019). Geological fate of seafloor massive sulphides at the TAG hydrothermal field (Mid-Atlantic Ridge). Ore Geology Reviews, 107, 903-925.
Singer, E., Emerson, D., Webb, E. A., Barco, R. A., Kuenen, J. G., Nelson, W. C., ... & Edwards, K. J. (2011). Mariprofundus ferrooxydans PV-1 the first genome of a marine Fe (II) oxidizing Zetaproteobacterium. PloS one, 6(9), e25386.
Slobodkina, G. B., Kolganova, T. V., Chernyh, N. A., Querellou, J., Bonch-Osmolovskaya, E. A., & Slobodkin, A. I. (2009a). Deferribacter autotrophicus sp. nov., an iron (III)-reducing bacterium from a deep-sea hydrothermal vent. Int. J. Syst. Evol. Microbiol., 59(6), 1508-1512.
Toner, B. M., Santelli, C. M., Marcus, M. A., Wirth, R., Chan, C. S., McCollom, T., ... & Edwards, K. J. (2009). Biogenic iron oxyhydroxide formation at mid-ocean ridge hydrothermal vents: Juan de Fuca Ridge. Geoch. & Cosmoch. Acta, 73(2), 388-403.
Hydrothermal ecosystems strongly rely on iron (Fe) rich substrates found at significant concentrations in sulfide minerals under a solid form such as pyrite, chalcopyrite, marcasite or pyrrhotite or in complexed minerals such as iron oxyhydroxides. The diversity and structure of microbial communities involved in the Fe-cycle in deep-sea hydrothermal vent ecosystems could strongly drive biomineralization and alteration of mineral structures and subsequently sustaining microbial communities. The spatial distribution of Fe species is widely shaped by the redox gradients characterizing this part of the geosphere. Consequently, Ferric Fe (Fe3+) is mainly used by chemoorganotroph prokaryotes as an electron acceptor under anaerobic conditions while ferrous Fe (Fe2+) is a chemical element structuring chemolithoautotrophic communities at acidic pH. Pathways involved in Fe3+-reducing and Fe2+-oxidizing metabolisms remain only partially resolved. To date, only a few Fe3+-reducing (hyper)thermophilic prokaryotes and Fe2+-oxidizing taxa have been isolated. However recent genomic studies of Zetaproteobacteria, provided new marker genes involved in Fe2+-oxidation characterizing the role of these microorganisms in deep-sea hydrothermal ecosystems such as an involvement in the alteration of Fe-rich minerals. Therefore, the main objective of the IRON2MI project is to cultivate microorganisms and to characterize metabolic pathways involved in Fe3+-reduction and Fe2+-oxidation in deep-sea hydrothermal ecosystems, and consequently their contribution to the alteration of Fe-rich minerals. State of the art cultivation technics, genomic approaches and in situ measurements applied to the study of deep-sea hydrothermal vent ecosystems at the Mid-Altantic Ridge will be used. Overall, these processes are of importance to understand the impact of deep-sea mining and the evolution of seafloor deposits.
Project coordination
Sophie Mieszkin (Université de Brest)
The author of this summary is the project coordinator, who is responsible for the content of this summary. The ANR declines any responsibility as for its contents.
Partnership
Université de Brest
Help of the ANR 292,406 euros
Beginning and duration of the scientific project:
September 2022
- 48 Months
