Under pressure: the diversity and physiology of the hydrothermal vent microbiome
Creators: name: Schlegel, Ian Jeremy
Publisher: name: No Publisher Supplied
Year: 2024

description: Hydrothermal vents form where warm, buoyant magma upwells from deep within the Earth and interacts across or through the crust with cold sea water. These phenomena occur globally, in all ocean basins, and in both shallow and deep water. Depending on the chemical composition of the magma or the rocks across which it interacts, there are several different vent chemistries that can ensue, but basalt hosted mafic vents are the most common. The derivative fluids form a unique chemical milieu enriched in reduced species of geological origin, while mixing with sea water sufficiently to present oxidants of sufficient strength to facilitate a habitat ~99% supported by autochthonous chemosynthesis, as opposed to the photosynthesis which facilitates the rest of the world’s trophic network. Simultaneously, as the majority of known hydrothermal vents occur in deep water, hydrostatic pressure imposes a unique set of opportunities and challenges biology must respond to in order to successfully colonize and persist within the habitat, yet hydrostatic pressure is the physical barrier condition least understood by biologists. Organisms can have one of three relationships to hydrostatic pressure; piezosensitivity, where growth is inhibited by hydrostatic pressure, piezotolerance, where growth is neither particularly supported or inhibited by hydrostatic pressure, or piezophily, where growth is stimulated by high pressure. As the cellular membranes are thought to be the parts of the cell most responsive to hydrostatic pressure, the so called ‘homeoviscous response’ or adaptations made by the cell to keep their membranes a liquid crystal are used to classify the organismal response to elevated hydrostatic pressure. The objectives of this dissertation are to ascertain the community structure and metabolism of chemosynthetic biofilms from a deep sea hydrothermal vent, how those properties change over time and across a redox gradient, interrogate the metabolism of a novel isolate from a deep sea hydrothermal vent under in situ and experimental conditions, and to investigate the relationship to elevated hydrostatic pressure in closely related organisms from hydrothermal vents to find markers for piezophily as opposed to piezotolerance. To do so, biofilms were collected from established natural substrates (basalt, animal exteriors) as well as pioneer populations from artificial colonizers across a redox gradient at a basalt hosted deep sea hydrothermal vent, and analyzed at the metagenomics and metaproteomic levels. Pioneer populations were overwhelmingly dominated by the family Campylobacterales within the Campylobacterota (aka Epsilonproteobacteria). Over time, the population diversified at both the taxonomic and physiological levels, both within the Epsilonproteobacteria and by the recruitment of additional populations, and there appears to be niche zonation across the geochemical gradient. The most important metabolic processes were carbon fixation via the reductive TCA cycle, sulfur/sulfide oxidation, and nitrate/nitrite reduction, though numerous other processes were expressed at the proteomic level at the time of sampling including (micro)aerobic respiration, hydrogen oxidation, and heavy metal detoxification. Subsequently, an isolate from one such biofilm was physiologically and genetically characterized and compared to the other members of the second family within the Epsilonprotoebacteria, the Nautiliales. Said isolate, Nautilia sp. strain PV-1, was found to be an obligate hydrogen oxidizing, carbon fixing, and nitrate and/or sulfur reducing thermophile, in broad concurrence with its close relatives. An integrated prophage was discovered, and efforts were made to induce it. However, this strain’s growth was also found to be highly stimulated by in situ pressures via growth in a high pressure chemostat, while not being dependent on elevated pressure for growth. As the only known piezophile among the Epsilonproteobacteria to date, and the second known facultative thermopiezophile, its closest relative at the 16S rRNA gene level, Nautilia abyssi strain PH1209T was also physiologically and genetically characterized, either to identify another piezophilic Epsilonproteobacterium, or to query the adaptations that define an organism as piezophilic or piezotolerant. While both organisms were found to be different strains of the same species, and largely exhibit corresponding metabolic and genomic similarity, strain PH1209T was found to be piezotolerant, rather than piezophilic, and to lack the integrated phage. The membrane lipid profiles of both organisms were investigated under a variety of growth conditions, and it was determined that strain PV-1 has a (thus far) unique homeoviscous response that contains some elements of the traditional ‘psychropiezophile’ response at the membrane level, and some elements of the canonical obligate thermopiezophile homeoviscous response. Thus, a tentative lipidomic definition of a facultative thermopiezophile can be put forth.