Chemosynthetic Fe-oxidizing communities are common at diffuse-flow hydrothermal vents throughout the world’s oceans. The foundational members of these communities are the Zetaproteobacteria, a class of Proteobacteria that is primarily associated with ecosystems fueled by ferrous iron, Fe(II). We report here the discovery of two new isolates of Zetaproteobacteria isolated from the Mid-Atlantic Ridge (TAG-1), and the Mariana back-arc (SV-108), that are unique in that they can utilize either Fe(II) or molecular hydrogen (H₂) as sole electron donor and oxygen as terminal electron acceptor for growth. Both strains precipitated Fe-oxyhydroxides as amorphous particulates. The cell doubling time on H₂ vs Fe(II) for TAG-1 was 14.1 vs 21.8 h, and for SV-108 it was 16.3 vs 20 h, and it appeared both strains could use either H₂ or Fe(II) simultaneously. The strains were close relatives, based on genomic analysis, and both possessed genes for the uptake NiFe-hydrogenase required for growth on H₂. These two strains belong to Zetaproteobacteria operational taxonomic unit 9 (ZetaOTU9). A meta-analysis of public databases found ZetaOTU9 was only associated with Fe(II)-rich habitats, and not in other environments where known H₂-oxidizers exist. These results expand the metabolic repertoire of the Zetaproteobacteria, yet confirm that Fe(II) metabolism is the primary driver of their physiology and ecology.

Anthropogenically-impacted environments offer the opportunity to discover novel microbial species and metabolisms, which may be undetectable in natural systems. Here, a combined metagenomic and geochemical study in Base Mine Lake, Alberta, Canada, which is the only oil sands end pit lake to date, revealed that nitrification was performed by members from Nitrosomonadaceae, Chloroflexi and unclassified Gammaproteobacteria “MBAE14.” While Nitrosomonadaceae and Chloroflexi groups were relatively abundant in the upper oxygenated zones, MBAE14 dominated the hypoxic hypolimnetic zones (approximately 30% of total microbial communities); MBAE14 was not detected in the underlying anoxic tailings. Replication rate analyses indicate that MBAE14 grew in metalimnetic and hypolimnetic water cap regions, most actively at the metalimnetic, ammonia/oxygen transition zone consistent with it putatively conducting nitrification. Detailed genomic analyses of MBAE14 evidenced both ammonia oxidation and denitrification into dinitrogen capabilities. However, the absence of known CO₂-fixation genes suggests a heterotrophic denitrifying metabolism. Functional marker genes of ammonia oxidation (amo and hao) in the MBAE14 genome are homologous with those conserved in autotrophic nitrifiers, but not with those of known heterotrophic nitrifiers. We propose that this novel MBAE14 inhabits the specific ammonia-rich, oxygen and labile organic matter-limited conditions occurring in Base Mine Lake which selectively favors mixotrophic coupled nitrifier denitrification metabolism. Our results highlight the opportunities to better constrain biogeochemical cycles from the application of metagenomics to engineered systems associated with extractive resource sectors.

The biogeochemistry of acid mine drainage (AMD) derived from waste rock associated sulphide mineral oxidation is relatively well characterized and linked to Acidithiobacillus spp.. However, little is understood about the microbial communities and sulphur cycling before AMD develops, key component on its prevention. This study aimed to examine circum-neutral mining impacted water (MIW) communities and its laboratory enrichments for sulphur oxidizing bacteria (SoxBac). MIW in situ microbial communities differed in diversity, structure and relative abundance consistent with site specific variations in total aqueous sulphur concentrations (TotS; ~2 to 17 mM), pH (3.67 – 7.34), and oxygen (22% - 93% saturation). However, the sulphur oxidizer, Halothiobacillus spp. dominated seven of the nine total SoxBac enrichment communities (~76 to ~100% relative abundance), spanning three of the four mines. Indeed, the presence and relative abundance of the identified sixteen known and five unclassified Halothiobacillus spp. here, were the important clustering determinants across parent MIW and enrichment communities. Further, the presence of Halothiobacillus spp. was associated with driving the pH < 4 in enrichment experiments, and the combination of specific Halothiobacillus spp. in the enrichments affected the observed acid to sulphate ratios indicating differential sulphur cycling. Halothiobacillus spp. also dominated the parent communities of the two acidic MIWs providing corroborating evidence for its active role in net acid generation within these waters. These results identify a putative indicator organism specific to mine tailings reservoirs and highlight the need for further study of tailings associated sulphur cycling for better mine management and environmental stewardship.

A soil bacterial consortium that was grown on diesel fuel and consisted of more than 10 members from different genera was maintained through repetitive sub-culturing and was utilized as a practical model to investigate a bacterial community that was continuously exposed to petroleum hydrocarbons. Through metagenomics analyses, consortium member isolation, growth assays and metabolite identification which supported the linkage of genomic data and functionality, two pioneering genera, Sphingobium and Pseudomonas, whose catabolic capabilities were differentiated, were found to be responsible for the creation of specialized ecological niches that were apparently occupied by other bacterial members for survival within the consortium. Co-existing genera, Achromobacter and Cupriavidus, maintained their existence in the consortium through metabolic dependencies by utilizing hydrocarbon biotransformation products of pioneer metabolism which was confirmed through growth tests and identification of biotransformation products of the isolated strains. Pioneering Sphingobium and Pseudomonas spp. utilized relatively water insoluble hydrocarbon parent compounds and facilitated the development of a consortium community structure that resulted in creation of niches in response to diesel fuel exposure which were created through the production of more water soluble biotransformation products available to co-colonizers. That these and other organisms were still present in the consortium after multiple transfers spanning 15 years, provided evidence for these ecological niches. Member survival through occupation of these niches led to robustness of each group within the multispecies bacterial community. Overall, these results contribute to our understanding of the complex ecological relationships that may evolve during prokaryotic hydrocarbon pollutant biodegradation. Importance There are few metagenome studies that have explored soil consortia maintained on a complex hydrocarbon substrate after the community interrelationships were formed. A soil bacterial consortium maintained on diesel fuel was utilized as a practical model to investigate bacterial community relationships through metagenomics analyses, consortium member isolation, growth assays and metabolite identification which supported the linkage of genomic data and functionality. Two pioneering genera were responsible for biodegradation of aromatics and alkanes by initiating biotransformation and thereby created specialized niches that were populated by other members. A model that represents these relationships was constructed which contributes to our understanding of the complex ecological relationships that evolve during prokaryotic hydrocarbon pollutant biodegradation.

Marine and lake snow is a continuous shower of mixed organic and inorganic aggregates falling from the upper water where primary production is substantial. These pelagic aggregates provide a niche for microbes that can exploit these physical structures and resources for growth, thus are local hot spots for microbial activity. However, processes underlying their formation remain unknown. Here, we investigated the role of chemical signaling between two co-occurring bacteria that each make up more than 10% of the community in iron-rich lakes aggregates (iron snow). The filamentous iron-oxidizing Acidithrix strain showed increased rates of Fe(II) oxidation when incubated with cell-free supernatant of the heterotrophic iron-reducing Acidiphilium strain. Amendment of Acidithrix supernatant to motile cells of Acidiphilium triggered formation of cell aggregates displaying similar morphology to those of iron snow. Comparative metabolomics enabled the identification of the aggregation-inducing signal, 2-phenethylamine, which also induced faster growth of Acidiphilium. We propose a model that shows rapid iron snow formation, and ultimately energy transfer from the photic zone to deeper water layers, is controlled via a chemically mediated interplay.