Life without light: Microbial diversity and evidence of sulfur- and ammonium-based chemolithotrophy in Movile Cave

Yin Chen, Liqin Wu, Rich Boden, Alexandra M Hillebrand-Voiculescu, Deepak Kumaresan, Hélène Moussard, Mihai Baciu, Yahai Lu, J Colin Murrell

Research output: Contribution to journalArticlepeer-review

160 Citations (Scopus)

Abstract

Microbial diversity in Movile Cave (Romania) was studied using bacterial and archaeal 16S rRNA gene sequence and functional gene analyses, including ribulose-1,5-bisphosphate carboxylase/oxygenase (RuBisCO), soxB (sulfate thioesterase/thiohydrolase) and amoA (ammonia monooxygenase). Sulfur oxidizers from both Gammaproteobacteria and Betaproteobacteria were detected in 16S rRNA, soxB and RuBisCO gene libraries. DNA-based stable-isotope probing analyses using 13 C-bicarbonate showed that Thiobacillus spp. were most active in assimilating CO 2 and also implied that ammonia and nitrite oxidizers were active during incubations. Nitrosomonas spp. were detected in both 16S rRNA and amoA gene libraries from the heavy DNA and sequences related to nitrite-oxidizing bacteria Nitrospira and Candidatus Nitrotoga were also detected in the heavy DNA, which suggests that ammonia/nitrite oxidation may be another major primary production process in this unique ecosystem. A significant number of sequences associated with known methylotrophs from the Betaproteobacteria were obtained, including Methylotenera, Methylophilus and Methylovorus, supporting the view that cycling of one-carbon compounds may be an important process within Movile Cave. Other sequences detected in the bacterial 16S rRNA clone library included Verrucomicrobia, Firmicutes, Bacteroidetes, alphaproteobacterial Rhodobacterales and gammaproteobacterial Xanthomonadales. Archaeal 16S rRNA sequences retrieved were restricted within two groups, namely the Deep-sea Hydrothermal Vent Euryarchaeota group and the Miscellaneous Crenarchaeotic group. No sequences related to known sulfur-oxidizing archaea, ammonia-oxidizing archaea, methanogens or anaerobic methane-oxidizing archaea were detected in this clone library. The results provided molecular biological evidence to support the hypothesis that Movile Cave is driven by chemolithoautotrophy, mainly through sulfur oxidation by sulfur-oxidizing bacteria and reveal that ammonia- and nitrite-oxidizing bacteria may also be major primary producers in Movile Cave.

Original languageEnglish
Pages (from-to)1093-1104
Number of pages12
JournalThe ISME Journal
Volume3
Issue number9
DOIs
Publication statusPublished - Sept 2009
Externally publishedYes

Keywords

  • Ammonia-oxidizing bacteria
  • DNA stable-isotope probing
  • Movile Cave
  • Sulfur-oxidizing bacteria

ASJC Scopus subject areas

  • Ecology, Evolution, Behavior and Systematics

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