Microbial social lives: a multi-scale approach to decoding microbial metabolic networks

Abstract

Microbial life exists everywhere on Earth, including below the surface. Caves provide an accessible view into subsurface microbial abundance. Without light or photosynthesis, cave microbial communities must rely on alternative carbon and energy sources. Methane, the most common hydrocarbon in the atmosphere, is a crucial energy and carbon source for cave ecosystems. In karst caves, methane is depleted due to the activity of methane-oxidizing bacteria (MOB), making these caves global methane sinks. Methane oxidation is particularly important in Movile Cave, an isolated ecosystem near the Black Sea, which has been sealed from surface inputs for ~5.5 million years. Despite its isolation, Movile Cave hosts a diverse ecosystem sustained entirely by chemolithoautotrophic carbon fixation.

Knowledge of MOB and methanogenic archaea distribution in caves is limited. An analysis of publically available shotgun metagenomes was used to assess methane cycling populations in cave ecosystems. It confirmed the dominance of USCγ clade MOB in karst caves and the widespread presence of Methanosarcina methanogens. While past studies of Movile Cave focused mainly on floating microbial mats, this work used metagenomics and geochemical techniques , x-ray diffraction (XRD), Fourier transformation infared spectroscopy (FTIR), scanning electron microscopy (SEM), and electron dispersive spectroscopy (EDAS) to characterise the community composition and geochemistry of other niches in Movile Cave, to expand understanding of how the ecosystem functions. Metagenomic analysis revealed a consistent presence of sulphur-oxidising bacteria (Thiobacillus) and the complete ammonia oxidation (comammox) capable Nitrospira across the cave. Functional analysis and enrichment experiments indicated widespread methane oxidation potential, especially in the wall biofilm, which showed high MOB abundance and particulate methane monooxygenase (pMMO). The microbial mat and biofilm also showed potential for carbon monoxide oxidation, supported by the presence of CODH genes and genomes. These findings expand our understanding of how Movile Cave functions as a methane-driven ecosystem.

Thesis is embargoed until 31st December 2029.

Date of Award	Dec 2024
Original language	English
Awarding Institution	Queen's University Belfast
Sponsors	NERC QUADRAT
Supervisor	Deepak Kumaresan (Supervisor), Rory Doherty (Supervisor) & Jean-Christophe Comte (Supervisor)