Genomic Diversity of Magnetotactic Bacteria from Underexplored Extreme Aquatic Habitats

Abstract

Magnetotactic bacteria (MTB) are metabolically versatile prokaryotes characterised by their ability to biomineralise intracellular magnetic nanocrystals within organelles called magnetosomes. These organelles assist MTB to align with geomagnetic field lines using magnetotaxis, thereby facilitating their navigation within chemically stratified aquatic environments. While the ecological and biogeochemical roles of MTB have been investigated extensively in freshwater and marine sediments, our understanding of their diversity, ecological function, and evolutionary significance in extreme and underexplored habitats remains limited. This doctoral research addresses these knowledge gaps by investigating MTB in two ecologically and geochemically distinct systems: acidic peatlands and oceanic oxygen minimum zones (OMZs). Using a multifaceted approach that integrates microbiological enrichment, high-resolution microscopy, and genome-resolved metagenomics, the taxonomic novelty, metabolic diversity, and adaptive strategies of MTB in these environments have been investigated here. In the first part of the thesis, MTB from the acidic Dajiuhu Peatland, located in the Shennongjia District of central China are investigated. This unique ecosystem, characterised by low pH (approximately pH of 4.0), high organic matter content, and pronounced redox stratification, provides a suitable niche for the discovery of a novel MTB strain, Magnetominusculus dajiuhuensis DJH-1Ts. The metabolic versatility of the strain allows it to thrive under anaerobic conditions while contributing to critical biogeochemical processes. Fluorescence in situ hybridisation with a species-specific probe further confirms the taxonomic and morphological identity of this novel strain. The genome-based taxonomy places M. dajiuhuensis within a new genus, Magnetominusculus, under the phylum Nitrospirota, which expands the phylogenetic breadth of known MTB. In the second part of the thesis, this investigation is extended to global oceanic OMZs, which are regions of suboxic to anoxic water columns where microbial communities exert strong control over nutrient dynamics. A total of 88 publicly available metagenomic datasets from OMZs were retrieved and processed. Using a combination of assembly, binning, and refinement tools, 30 MGC-containing bacterial metagenome-assembled genomes (MAGs) were recovered. These MAGs belong to diverse taxonomic lineages across 14 phylum-level classifications, including groups known to contain MTB as well as novel lineages previously not found to harbour MTB. Functional annotation reveals a variety of MGC architectures containing genes involved in nitrogen and sulphur metabolism. Kyoto Encyclopedia of Genes and Genomes (KEGG) pathway reconstructions and comparative genomic analyses suggest that these OMZ-derived potential MGC-containing bacteria maybe involved in denitrification, sulphate reduction, and carbon fixation under low-oxygen conditions, thereby playing a pivotal role in regulating oceanic redox processes. Computational pipelines were used for genome annotation, phylogenomics, and metabolic reconstruction. MGC screening was conducted using MagCluster, with annotations cross-verified via PSI-BLAST and visualised using clinker. The discovery of MTB in peatlands adds to previous findings of MTB from the Dajiuhu Peatland, albeit with extensive and more thorough morphological and genomic characterisation; while the prevalence of MGC-containing bacteria (putative MTB) in OMZs underscores their capacity to adapt to low-oxygen marine environments. The utility of genome-resolved metagenomics in uncovering hidden microbial diversity and biogeochemical function in complex ecosystems is also underscored, which might otherwise go unnoticed. Show more