title: Metagenomic study of red biofilms from Diamante Lake reveals ancient arsenic bioenergetics in haloarchaea.
abstract: Arsenic metabolism is proposed to be an ancient mechanism in microbial life. Different bacteria and archaea use detoxification processes to grow under high arsenic concentration. Some of them are also able to use arsenic as a bioenergetic substrate in either anaerobic arsenate respiration or chemolithotrophic growth on arsenite. However, among the archaea, bioenergetic arsenic metabolism has only been found in the Crenarchaeota phylum. Here we report the discovery of haloarchaea (Euryarchaeota phylum) biofilms forming under the extreme environmental conditions such as high salinity, pH and arsenic concentration at 4589 m above sea level inside a volcano crater in Diamante Lake, Argentina. Metagenomic analyses revealed a surprisingly high abundance of genes used for arsenite oxidation (aioBA) and respiratory arsenate reduction (arrCBA) suggesting that these haloarchaea use arsenic compounds as bioenergetics substrates. We showed that several haloarchaea species, not only from this study, have all genes required for these bioenergetic processes. The phylogenetic analysis of aioA showed that haloarchaea sequences cluster in a novel and monophyletic group, suggesting that the origin of arsenic metabolism in haloarchaea is ancient. Our results also suggest that arsenite chemolithotrophy likely emerged within the archaeal lineage. Our results give a broad new perspective on the haloarchaea metabolism and shed light on the evolutionary history of arsenic bioenergetics.
authors.affiliation: Instituto de Agrobiotecnología de Rosario (INDEAR), Ocampo 210 bis (2000), Predio CCT Rosario, Santa Fe, Argentina.
authors.forename: Nicolás
authors.initials: N
authors.lastname: Rascovan
authors.affiliation: Laboratorio de Investigaciones Microbiológicas de Lagunas Andinas (LIMLA), Planta Piloto de Procesos Industriales Microbiológicos (PROIMI), CCT, CONICET, San Miguel de Tucumán, Tucumán, Argentina.
authors.forename: Javier
authors.initials: J
authors.lastname: Maldonado
authors.affiliation: Instituto de Agrobiotecnología de Rosario (INDEAR), Ocampo 210 bis (2000), Predio CCT Rosario, Santa Fe, Argentina.
authors.forename: Martín P
authors.initials: MP
authors.lastname: Vazquez
authors.affiliation: Laboratorio de Investigaciones Microbiológicas de Lagunas Andinas (LIMLA), Planta Piloto de Procesos Industriales Microbiológicos (PROIMI), CCT, CONICET, San Miguel de Tucumán, Tucumán, Argentina.
authors.forename: María
authors.initials: M
authors.lastname: Eugenia Farías
mesh_terms: D001105:Archaea / Q000145:classification / Q000235:genetics / Q000302:isolation & purification* / Q000502:physiology*; D001149:Arsenates / Q000378:metabolism*; D001151:Arsenic / Q000378:metabolism; D018053:Arsenites / Q000378:metabolism; D018441:Biofilms; D052837:Chemoautotrophic Growth; D004734:Energy Metabolism; D060106:Lakes / Q000382:microbiology*; D056186:Metagenomics; D008969:Molecular Sequence Data; D010084:Oxidation-Reduction; D010802:Phylogeny
chemical_list: D001149:Arsenates; D018053:Arsenites; C015001:arsenite; D001151:Arsenic; C025657:arsenic acid