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Hinrichs, K.-U.

Publications and source records attributed to Hinrichs, K.-U..

7 recordsLinked to original sources

Novel Extended Tetraether Lipids Found in a High-CO2 Geyser

The growing research into the archaeal lipidome has uncovered a remarkable structural diversity in glycerol dialkyl glycerol tetraethers (GDGTs) and revealed complex membrane adaptations, especially in extreme environments. We performed a comprehensive analysis of the lipidome from the subsurface water of a CO2-rich, cold-water Geyser Andernach (Germany), using ultra-high-resolution mass spectrometry methods. We detected GDGT-0, presumably derived from the dominant community member Candidatus Altiarchaeum, providing evidence for its ability to synthesize tetraethers as previously predicted from metagenomic data. Beyond the typical GDGT-0 and acyclic glycerol trialkyl glycerol tetraether (GTGT-0), we discovered novel structural analogues, here referred to as extended GDGTs and GTGTs, characterized by the asymmetrical addition of up to two isoprenoid units to only one of their hydrocarbon side chains, analogous to those found in extended archaeols. The lack of GDGT ring synthase A (GrsA) and GrsB homologs in the corresponding metagenome-assembled genome, suggests that the producing archaeon may utilize extended GDGTs as a membrane adaptation to cope with the energy-depleted conditions of the geyser environment, highlighting the adaptive flexibility of archaea to extreme physicochemical conditions.

biochemistry↗

Metabolic controls on the carbon isotope fractionations of bacterial fermentation

Microbial fermentation facilitates the initial breakdown of organic matter into small molecules, and is thought to be the rate-limiting step for mineralization under anoxic conditions. Fermentation is understudied in modern and ancient biogeochemistry due to a lack of environmental biomarkers that would constrain its activity. It has long been assumed that fermentation, like respiration, does not express significant carbon isotope fractionations, precluding isotopic signals as a means of studying it in nature. Here, we tested this idea by growing pure cultures of four fermenting bacteria on glucose and measuring the carbon isotope compositions of the organic acids and alcohols produced. We found that fermentation exhibits a strong carbon isotope fractionation, ranging from -6{per thousand} to +16{per thousand}, depending on the fermentation product. This range can even be observed within a single organism. Using bioisotopic models that track site-specific isotope enrichments through metabolic networks, we constrained the enzymes responsible for these fractionations. Our models reproduced in vivo organic acid{delta} 13C values in all four organisms. These findings demonstrate that acetate 13C-enrichment is likely a consistent signature of fermentation. Furthermore, our study suggests that fermentation imposes an anaerobic trophic carbon isotope fractionation as organic carbon is passed from fermenters to secondary degraders like sulfate reducers. Looking to the geologic past, this trophic fractionation could have imprinted isotopic signals on the three billion year record of sedimentary organic carbon, specifically the inverse{delta} 13C pattern of Precambrian acyclic isoprenoid and n-alkane biomarkers. Pervasive evidence of fermentation in the rock record suggests its under-appreciated role in biogeochemical cycles throughout Earth history. Significance StatementMicroorganisms drive the global cycling of elements like carbon and regulate the Earths climate on both human and geologic timescales. Of particular importance is the microbial breakdown of organic matter, which generates greenhouse gases like methane. Fermenting bacteria play a crucial role in anaerobic carbon degradation. However, they remain largely invisible to our analyses. We explored the natural abundance of carbon stable isotopes in the molecular products of fermentation as a tool to study this metabolism in modern ecosystems and the ancient biosphere. We identified significant isotopic signals in molecules produced by fermenting bacteria and compared them to previously observed isotopic signals in molecular fossils in sedimentary rocks, which may provide evidence of microbial fermentation on the Precambrian Earth.

microbiology↗

A novel quinone biosynthetic pathway illuminates the evolution of aerobic metabolism

The dominant organisms in modern oxic ecosystems rely on respiratory quinones with high redox potential (HPQs) for electron transport in aerobic respiration and photosynthesis. The diversification of quinones, from low redox potential in anaerobes to HPQs in aerobes, is assumed to have followed Earths surface oxygenation [~]2.3 billion years ago. However, the evolutionary origins of HPQs remain unresolved. Here, we characterize the structure and biosynthetic pathway of a novel ancestral HPQ, methyl-plastoquinone, that is unique to bacteria of the phylum Nitrospirota. Methyl-plastoquinone is structurally related to the two previously known HPQs, plastoquinone from Cyanobacteriota/chloroplasts and ubiquinone from Pseudomonadota/mitochondria, respectively. We demonstrate a common origin of the three HPQ biosynthetic pathways that predates the emergence of Nitrospirota, Cyanobacteriota, and Pseudomonadota. An ancestral HPQ biosynthetic pathway evolved [≥] 3.4 billion years ago in an extinct lineage and was laterally transferred to these three phyla [~]2.5-3.2 billion years ago. We show that Cyanobacteriota and Pseudomonadota were ancestrally aerobic and thus propose that aerobic metabolism using HPQs significantly predates Earths surface oxygenation. Two of the three HPQ pathways were later obtained by eukaryotes through endosymbiosis forming chloroplasts and mitochondria, enabling their rise to dominance in modern oxic ecosystems. Significance statementOxygenic photosynthesis and aerobic respiration by bacteria and eukaryotes rely on respiratory quinones with high redox potential that facilitate membrane-bound electron transport. These quinones are integral to aerobic metabolism and therefore the evolution of aerobic metabolism and quinone biosynthesis must be intertwined. Only two types of high redox potential quinones have been described in bacteria and eukaryotes. Here, we describe the structure and biosynthetic pathway of a third type, methyl-plastoquinone, that is exclusive to bacteria of the phylum Nitrospirota. We then use phylogenetic analysis to show that the three high redox potential quinones have a single evolutionary origin and are much older than previously considered, predating the Great Oxygenation Event, when significant amounts of O2 first accumulated in the atmosphere.

microbiology↗

Unravelling Plankton Adaptation in Global Oceans through the Analysis of Lipidomes

A recent global survey of planktonic lipids showed a fundamental temperature-mediated regulation of lipid unsaturation in the global oceans [Holm H, et al. (2022) Science 376:1487-1491]. We expand the analysis of this dataset, both spatially and methodologically, to examine diverse environmental stressors across the ocean. Utilizing weighted correlation network analysis, we analyzed 3,164 lipid features in the dataset comprising 930 samples of suspended particulate matter, taken across a broad range of oceanographic conditions and water depths up to 600 meters. A total of 16 lipid clusters being co-expressed across diverse environments were identified. This analysis reveals universal relationships between environmental factors and the lipidome of the planktonic community. The largest lipid cluster, comprising 481 lipid features, including glycerolipids with polyunsaturated fatty acids, exhibited a significant enrichment in polar oceans, suggesting the highest lipid diversity in these ocean regions. Remarkably, marine plankton in these regions employ both desaturation and chain shortening for cold acclimation. Additionally, one lipid cluster strongly linked to the plankton residing in the surface of tropical and subtropical oceans was enriched with non-phosphorus lipids. We suggest this adaptive response enables the plankton to cope with phosphorous scarcity and heat stress. Notably, in the subsurface of these regions, a co-expressed cluster of highly unsaturated lipids is consistent with an enhanced production of polyunsaturated fatty acids by phytoplankton, possibly for low light adaptation. This adaptation is important as it may represent a source of essential fatty acids below the warm sea surface where such vital compounds may be diminished in the warmer future. SignificanceMarine plankton is vital for marine ecosystems and climate regulation. We analyzed a large lipidomics dataset of 930 samples collected from global oceans. This allowed us to explore how plankton adapt their lipidomes across different environments. Our findings show distinct lipid clusters correlating with specific environmental conditions, revealing mechanisms like chain shortening to cope with cold stress, enrichment of non-phosphorus lipids in tropical surface waters, and increased polyunsaturated fatty acids in low-light tropical subsurface areas. These adaptations are crucial for understanding how climate change will impact marine ecosystems.

microbiology↗

A 2-million-year-old microbial and viral communities from the Kap Kobenhavn Formation in North Greenland

Environmental DNA (eDNA) from the 2-million-year-old Kap Kobenhavn Formation of northern Greenland has revealed an ecosystem of plants and animals with no contemporary analogue1. Here, we reconstruct the microbial (bacterial, archaeal, and viral) communities that thrived at the site during this time. By leveraging a novel analytical framework that integrates taxonomic profiling, DNA damage estimates, and functional reconstructions, we identify and distinguish pioneer microbial communities from later permafrost microbial assemblages. We show that at the time of sediment deposition, the terrestrial input at the Kap Kobenhavn site originated from a palustrine wetland, suggesting warmer, non-permafrost conditions. During this period, the detection of methanogenic archaea and signals of their carbon metabolism is consistent with Kap Kobenhavn and similar northern ecosystems contributing moderate methane emissions. Intriguingly, we discover a remarkable nucleotide sequence similarity--exceeding 98%--between pioneer methanogens and present-day analogues in thawing permafrost. This aligns with the concept of "time-traveling" microbes2 surviving across geological time and waiting for conditions to turn favourable rather than evolving to adapt to changing conditions. Importantly, in contrast to the plant and animal communities of the Kap Kobenhavn, a striking similarity in microbial composition to that of a contemporary thawing Arctic suggests that microbial communities may serve as the first indication of broader climate-driven ecosystem disruptions.

microbiology↗

The exploration of Thermococcus barophilus lipidome reveals the widest variety of phosphoglycolipids in Thermococcales.

One of the most distinctive characteristics of Archaea is their unique lipids. While the general nature of archaeal lipids has been linked to their tolerance to extreme conditions, little is known about the diversity of lipidic structures Archaea are able to synthesize, which hinders the elucidation of the physicochemical properties of their cell membrane. In an effort to widen the known lipid repertoire of the piezophilic and hyperthermophilic model archaeon Thermococcus barophilus, we comprehensively characterized its intact polar lipid (IPL), core lipid (CL), and polar head group compositions using a combination of cutting-edge liquid chromatography and mass spectrometric ionization systems. We tentatively identified 82 different IPLs based on five distinct CLs and 10 polar head group derivatives of phosphatidylhexoses, including compounds reported here for the first time, e.g., di-N-acetylhexosamine phosphatidylhexose-bearing lipids. Despite having extended the knowledge on the lipidome, our results also indicate that the majority of T. barophilus lipids remain inaccessible to current analytical procedures and that improvements in lipid extraction and analysis are still required. This expanded yet incomplete lipidome nonetheless opens new avenues for understanding the physiology, physicochemical properties, and organization of the membrane in this archaeon as well as other Archaea.

microbiology↗

Lipid analysis of CO2-rich subsurface aquifers suggests an autotrophy-based deep biosphere with lysolipids enriched in CPR bacteria

Sediment-hosted CO2-rich aquifers deep below the Colorado Plateau (USA) contain a remarkable diversity of uncultivated microorganisms, including Candidate Phyla Radiation (CPR) bacteria that are putative symbionts unable to synthesize membrane lipids. The origin of organic carbon in these ecosystems is unknown and the source of CPR membrane lipids remains elusive. We collected cells from deep groundwater brought to the surface by eruptions of Crystal Geyser, sequenced the community, and analyzed the whole community lipidome over time. Characteristic stable carbon isotopic compositions of microbial lipids suggest that bacterial and archaeal CO2 fixation ongoing in the deep subsurface provides organic carbon for the complex communities that reside there. Coupled lipidomic-metagenomic analysis indicates that CPR bacteria lack complete lipid biosynthesis pathways but still possess regular lipid membranes. These lipids may therefore originate from other community members, which also adapt to high in situ pressure by increasing fatty acid unsaturation. An unusually high abundance of lysolipids attributed to CPR bacteria may represent an adaptation to membrane curvature stress induced by their small cell sizes. Our findings provide new insights into the carbon cycle in the deep subsurface and suggest the redistribution of lipids into putative symbionts within this community.

microbiology↗