Community genomic analysis of an extremely acidophilic sulfur-oxidizing biofilm

Abstract

Highly acidic (pH 0-1) biofilms, known as 'snottites', form on the walls and ceilings of hydrogen sulfide-rich caves. We investigated the population structure, physiology and biogeochemistry of these biofilms using metagenomics, rRNA methods and lipid geochemistry. Snottites from the Frasassi cave system (Italy) are dominated (470% of cells) by Acidithiobacillus thiooxidans, with smaller populations including an archaeon in the uncultivated 'G-plasma' clade of Thermoplasmatales (415%) and a bacterium in the Acidimicrobiaceae family (45%). Based on metagenomic evidence, the Acidithiobacillus population is autotrophic (ribulose-1,5-bisphosphate carboxylase/ oxygenase (RuBisCO), carboxysomes) and oxidizes sulfur by the sulfide-quinone reductase and sox pathways. No reads matching nitrogen fixation genes were detected in the metagenome, whereas multiple matches to nitrogen assimilation functions are present, consistent with geochemical evidence, that fixed nitrogen is available in the snottite environment to support autotrophic growth. Evidence for adaptations to extreme acidity include Acidithiobacillus sequences for cation transporters and hopanoid synthesis, and direct measurements of hopanoid membrane lipids. Based on combined metagenomic, molecular and geochemical evidence, we suggest that Acidithiobacillus is the snottite architect and main primary producer, and that snottite morphology and distributions in the cave environment are directly related to the supply of C, N and energy substrates from the cave atmosphere.

Metagenomic resolution of microbial functions in deep-sea hydrothermal plumes across the Eastern Lau Spreading Center

“…Metabolic versatility associated with sulfur oxidation may impart functional redundancy (Allison and Martiny, 2008) for sulfur oxidation in ELSC plumes, similar to other sulfur-dominated systems (Jones et al, 2012). The diversity and versatility of sulfuroxidizing microorganisms that are abundant both in ELSC plumes and in surrounding waters could make sulfur oxidation resilient in the dynamic setting of deep-sea hydrothermal plumes, allowing it to persist during long periods between sulfur availability.…”

Making a living while starving in the dark: metagenomic insights into the energy dynamics of a carbonate cave

“…Avenues for understanding alternate non-photosynthetic primary production strategies are limited to subterranean or deep-sea ecosystems that function in the absence of sunlight. A significant amount of research has been devoted to characterizing primary production in ecosystems such as hydrothermal vents (reviewed by Nakagawa and Takai, 2008) and sulfidic caves (Sarbu et al, 1996;Chen et al, 2009;Engel et al, 2010;Jones et al, 2012), where supplies of reduced sulfur, hydrogen or methane support rich chemolithoautotophic activity; however, the energy dynamics of carbonate caves are less well defined. Carbonate cave communities are presumed to be sustained by allocthonous carbon sourced from photic surface ecosystems and entering the cave with vadose-zone drip water, surface water flow or the behavior of macrofauna (Laiz et al, 1999;Simon et al, 2003;Barton et al, 2004).…”

Metagenomics of extreme environments

“…Highly acidic (pH 0-1) biofilms ("snottites") were recently investigated using metagenomic sequencing [50]. In contrast to the AMD biofilms, these are largely dominated by Acidithiobacillus thiooxidans, Acidimicrobium and Ferrimicrobium spp.…”