Aerobic proteobacterial methylotrophs in Movile Cave: genomic and metagenomic analyses - PubMed (original) (raw)

Aerobic proteobacterial methylotrophs in Movile Cave: genomic and metagenomic analyses

Deepak Kumaresan et al. Microbiome. 2018.

Abstract

Background: Movile Cave (Mangalia, Romania) is a unique ecosystem where the food web is sustained by microbial primary production, analogous to deep-sea hydrothermal vents. Specifically, chemoautotrophic microbes deriving energy from the oxidation of hydrogen sulphide and methane form the basis of the food web.

Results: Here, we report the isolation of the first methane-oxidizing bacterium from the Movile Cave ecosystem, Candidatus Methylomonas sp. LWB, a new species and representative of Movile Cave microbial mat samples. While previous research has suggested a prevalence of anoxic conditions in deeper lake water and sediment, using small-scale shotgun metagenome sequencing, we show that metabolic genes encoding enzymes for aerobic methylotrophy are prevalent in sediment metagenomes possibly indicating the presence of microoxic conditions. Moreover, this study also indicates that members within the family Gallionellaceae (Sideroxydans and Gallionella) were the dominant taxa within the sediment microbial community, thus suggesting a major role for microaerophilic iron-oxidising bacteria in nutrient cycling within the Movile Cave sediments.

Conclusions: In this study, based on phylogenetic and metabolic gene surveys of metagenome sequences, the possibility of aerobic microbial processes (i.e., methylotrophy and iron oxidation) within the sediment is indicated. We also highlight significant gaps in our knowledge on biogeochemical cycles within the Movile Cave ecosystem, and the need to further investigate potential feedback mechanisms between microbial communities in both lake sediment and lake water.

Keywords: Extreme ecosystem; Methane; Methanotrophs; Methylotrophic bacteria; Movile cave; One-carbon metabolism.

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Figures

Fig. 1

Fig. 1

Phylogenetic neighbour-joining trees of (a) 16S rRNA gene sequences showing the relationship between the MOB isolate from Movile Cave to other members within the genus Methylomonas and Methylococcus capsulatus Bath. b Partial PmoA sequences amplified from the isolate LWB and other closely related PmoA sequences with the ammonia monooxygenase (AmoA) sequence as an out-group. Scale bar = 0.1 change per base position, (c) partial MmoX sequences derived from the MOB isolate genome and other closely related MmoX sequences with the butane monooxygenase (BmoX) sequence as an out-group. Scale bar = 0.01 change per base position

Fig. 2

Fig. 2

Comparison of relative abundance (normalized to RecA abundance) of different metabolic genes sequences in mat and sediment metagenomes. For one-carbon cycling: pmoA (particulate methane monooxygenase), mmox (soluble methane monoxygenase), mxaF/xoxF (methanol dehydrogenases), gmaS (gamma-glutamylmethylamide synthetase), mauA (methylamine dehydrogenase) and mcrA (methyl coenzyme M reductase)

Fig. 3

Fig. 3

An approximately maximum-likelihood tree constructed using partial MmoX peptide sequences retrieved from the microbial mat metagenome, ratified MmoX peptide sequences (represented by blue font) and MmoX peptide sequence from the Methylomonas isolate from Movile Cave. Nodes with only MmoX peptide sequences from the microbial mat metagenomes are collapsed (grey triangles). Scale bar = 1 change per base position

Fig. 4

Fig. 4

An approximately maximum-likelihood tree constructed using partial GmaS peptide sequences retrieved from both microbial mat and sediment metagenomes, ratified GmaS peptide sequences (represented in blue font), and both Movile Cave isolates (represented in red font) and environmental GmaS (represented in green font) peptide sequences. Nodes with GlnA (glutamine synthetase) peptide sequences are represented by purple colour. Nodes with only MxaF/XoxF peptide sequences from the microbial mat metagenomes are collapsed (triangles). Scale bar = 1 change per base position

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