First description of giant Archaea (Thaumarchaeota) associated with putative bacterial ectosymbionts in a sulfidic marine habitat

Authors

  • Félix Muller,

    Corresponding author
    1. Université des Antilles et de la Guyane UFR des Sciences Exactes et Naturelles Département de Biologie, BP 592. 97159 Pointe-à-Pitre cedex, Guadeloupe, France.
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  • Terry Brissac,

    1. Université des Antilles et de la Guyane UFR des Sciences Exactes et Naturelles Département de Biologie, BP 592. 97159 Pointe-à-Pitre cedex, Guadeloupe, France.
    2. Université Pierre et Marie Curie, Bat. A, 4èmeétage, 7 quai St Bernard, 75005 Paris, France.
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  • Nadine Le Bris,

    1. Université Pierre et Marie Curie, Banyuls-sur-Mer 66650, Paris, France.
    2. Laboratoire Environnement Profond, Zone de la Pointe du Diable, BP70, 29280 Plouzané, France.
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  • Horst Felbeck,

    1. Scripps Institution of Oceanography, University of California San Diego, La Jolla, California 92093-0202, USA.
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  • Olivier Gros

    1. Université des Antilles et de la Guyane UFR des Sciences Exactes et Naturelles Département de Biologie, BP 592. 97159 Pointe-à-Pitre cedex, Guadeloupe, France.
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E-mail fmuller@univ-ag.fr; Tel. (+590) 590 48 30 06; Fax (+590) 590 48 30 06.

Summary

Archaea may be involved in global energy cycles, and are known for their ability to interact with eukaryotic species (sponges, corals and ascidians) or as archaeal–bacterial consortia. The recently proposed phylum Thaumarchaeota may represent the deepest branching lineage in the archaeal phylogeny emerging before the divergence between Euryarchaeota and Crenarchaeota. Here we report the first characterization of two marine thaumarchaeal species from shallow waters that consist of multiple giant cells. One species is coated with sulfur-oxidizing γ-Proteobacteria. These new uncultured thaumarchaeal species are able to live in the sulfide-rich environments of a tropical mangrove swamp, either on living tissues such as roots or on various kinds of materials such as stones, sunken woods, etc. These archaea and archaea/bacteria associations have been studied using light microscopy, transmission electron microscopy and scanning electron microscopy. Species identification of archaeons and the putative bacterial symbiont have been assessed by 16S small subunit ribosomal RNA analysis. The sulfur-oxidizing ability of the bacteria has been assessed by genetic investigation on alpha-subunit of the adenosine-5′-phosphosulfate reductase/oxidase's (AprA). Species identifications have been confirmed by fluorescence in situ hybridization using specific probes designed in this study. In this article, we describe two new giant archaeal species that form the biggest archaeal filaments ever observed. One of these species is covered by a specific biofilm of sulfur-oxidizing γ-Proteobacteria. This study highlights an unexpected morphological and genetic diversity of the phylum Thaumarchaeota.

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