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The vent crab, Xenograpsus testudinatus ( xt crab), is adapted to inhabit shallow-water, high sulfide and hypoxic hydrothermal vent. Our previous study revealed sulfide tolerance of vent xt crabs which sulfide: quinone oxidoreductase ( xt SQR) paralogs aid in sulfide detoxification. However, the mechanisms of how xt crab adapts to high sulfide-hypoxic conditions in the vent area remain to be explored. In the present study, we tested the tolerance of xt crab to sulfide-induced hypoxia, and investigated their aerobic and anaerobic responses in situ and in the laboratory. Comparisons were made to a non-vent, intertidal species, Thranita danae ( td crab). We analyzed the several factors related to aerobic metabolism (SQR, cytochrome c [CYTC], complex IV [COXIV]), the product of anaerobic metabolism (hemolymph lactate levels) and glucose levels. Our results showed a higher survival tolerance to hypoxia of xt crabs than td crabs. Hemolymph lactate levels increased more rapidly in xt crabs than td crabs exposed to experimental hypoxia, revealing a rapid induction of anaerobic metabolism in hypoxic xt crabs. Lactate measurement in xt crabs returned from aquaria to original capture sites (vent habitats), further assessed the remarkable ability of xt crabs to rapidly switch on and off their anaerobic metabolism. To assess aerobic metabolism, long-term exposure of xt crabs to hydrothermal vent habitat increased gill xt CYTC transcripts and protein levels together with steadily enzymatic activity of COXIV. This revealed ability of xt crabs to maintain functional capacity of aerobic respiration in hypoxia. Phylogenetic analysis showed that xt SQR paralogs in xt crabs were more distant compared to td SQR paralogs in td crabs. The increase of transcripts and enzymatic activity of gill xt SQR, and co-localization of xt SQR and xt CYTC also contribute to maintain aerobic metabolism by preventing sulfide toxicity on mitochondrial respiratory function. Overall, our study suggests that multiple strategies including detoxification of sulfide by gill xt SQR, and a quick/dynamic switch between aerobic and anaerobic metabolisms may play important roles in the metabolic adaptations of xt crabs to extreme hydrothermal vent environment.

Soils represent the largest carbon reservoir within terrestrial ecosystems. The mechanisms controlling the amount of carbon stored and its feedback to the climate system, however, remain poorly resolved. Global carbon models assume that carbon cycling in upland soils is entirely driven by aerobic respiration; the impact of anaerobic microsites prevalent even within well-drained soils is missed within this conception. Here, we show that anaerobic microsites are important regulators of soil carbon persistence, shifting microbial metabolism to less efficient anaerobic respiration, and selectively protecting otherwise bioavailable, reduced organic compounds such as lipids and waxes from decomposition. Further, shifting from anaerobic to aerobic conditions leads to a 10-fold increase in volume-specific mineralization rate, illustrating the sensitivity of anaerobically protected carbon to disturbance. The vulnerability of anaerobically protected carbon to future climate or land use change thus constitutes a yet unrecognized soil carbon–climate feedback that should be incorporated into terrestrial ecosystem models. Mechanisms controlling soil carbon storage and feedbacks to the climate system remain poorly constrained. Here, the authors show that anaerobic microsites stabilize soil carbon by shifting microbial metabolism to less efficient anaerobic respiration and protecting reduced organic compounds from decomposition.

Waterlogging is one of the main abiotic stresses suffered by plants. Inhibition of aerobic respiration during waterlogging limits energy metabolism and restricts growth and a wide range of developmental processes, from seed germination to vegetative growth and further reproductive growth. Plants respond to waterlogging stress by regulating their morphological structure, energy metabolism, endogenous hormone biosynthesis, and signaling processes. In this updated review, we systematically summarize the changes in morphological structure, photosynthesis, respiration, reactive oxygen species damage, plant hormone synthesis, and signaling cascades after plants were subjected to waterlogging stress. Finally, we propose future challenges and research directions in this field.

A pathway triggered by chronic severe hypoxia boosts regeneration of injured hearts in adult mice. Hypoxia pathway linked to heart regeneration Hesham Sadek and colleagues show that a pathway triggered by chronic severe hypoxia boosts the regeneration of injured hearts in adult mice. Mice subjected to myocardial infarction that are placed in a hypoxic environment for a prolonged period make new cardiomyocytes, and recover heart function through a mechanism involving a reduction of reactive oxygen species concentration and cardiomyocyte cell cycle re-entry. Prolonged severe hypoxia is not a viable therapeutic strategy for use in humans, but targeting this pathway can induce myocardial regeneration. The adult mammalian heart is incapable of regeneration following cardiomyocyte loss, which underpins the lasting and severe effects of cardiomyopathy. Recently, it has become clear that the mammalian heart is not a post-mitotic organ. For example, the neonatal heart is capable of regenerating lost myocardium 1 , and the adult heart is capable of modest self-renewal 2 , 3 . In both of these scenarios, cardiomyocyte renewal occurs via the proliferation of pre-existing cardiomyocytes, and is regulated by aerobic-respiration-mediated oxidative DNA damage 4 , 5 . Therefore, we reasoned that inhibiting aerobic respiration by inducing systemic hypoxaemia would alleviate oxidative DNA damage, thereby inducing cardiomyocyte proliferation in adult mammals. Here we report that, in mice, gradual exposure to severe systemic hypoxaemia, in which inspired oxygen is gradually decreased by 1% and maintained at 7% for 2 weeks, results in inhibition of oxidative metabolism, decreased reactive oxygen species production and oxidative DNA damage, and reactivation of cardiomyocyte mitosis. Notably, we find that exposure to hypoxaemia 1 week after induction of myocardial infarction induces a robust regenerative response with decreased myocardial fibrosis and improvement of left ventricular systolic function. Genetic fate-mapping analysis confirms that the newly formed myocardium is derived from pre-existing cardiomyocytes. These results demonstrate that the endogenous regenerative properties of the adult mammalian heart can be reactivated by exposure to gradual systemic hypoxaemia, and highlight the potential therapeutic role of hypoxia in regenerative medicine.

Clinically, it is difficult to endow implants with excellent osteogenic ability and antibacterial activity simultaneously. Herein, the self-activating implants modified with hydroxyapatite (HA)/MoS 2 coating are designed to prevent Staphylococcus aureus ( S. aureus ) and Escherichia coli ( E. coli ) infections and accelerate bone regeneration simultaneously. The electron transfer between bacteria and HA/MoS 2 is triggered when bacteria contacted with the material. RNA sequencing data reveals that the expression level of anaerobic respiration–related genes is up-regulated and the expression level of aerobic respiration–related genes is down-regulated when bacteria adhere to the implants. HA/MoS 2 presents a highly effective antibacterial efficacy against both S. aureus and E. coli because of bacterial respiration–activated metabolic pathway changes. Meanwhile, this coating promotes the osteoblastic differentiation of mesenchymal stem cells by altering the potentials of cell membrane and mitochondrial membrane. The proposed strategy exhibits great potential to endow implants with self-activating anti-infection performance and osteogenic ability simultaneously. Bone implants with antibacterial and osteogenic properties are important for clinical applications, but creating both properties simultaneously remains challenging. Here, the authors demonstrate a self-activating implant using a hydroxyapatite and molybdenum disulfide coating which accelerates bone regeneration and at the same time prevents bacterial infection.

Abstract Oxygen (O2) is the ultimate oxidant on Earth and its respiration confers such an energetic advantage that microorganisms have evolved the capacity to scavenge O2 down to nanomolar concentrations. The respiration of O2 at extremely low levels is proving to be common to diverse microbial taxa, including organisms formerly considered strict anaerobes. Motivated by recent advances in O2 sensing and DNA/RNA sequencing technologies, we performed a systematic review of environmental metatranscriptomes revealing that microbial respiration of O2 at nanomolar concentrations is ubiquitous and drives microbial activity in seemingly anoxic aquatic habitats. These habitats were key to the early evolution of life and are projected to become more prevalent in the near future due to anthropogenic-driven environmental change. Here, we summarize our current understanding of aerobic microbial respiration under apparent anoxia, including novel processes, their underlying biochemical pathways, the involved microorganisms, and their environmental importance and evolutionary origin. The discovery of microbial oxygen respiration at and below the oxygen detection limit is changing our understanding of biogeochemical cycling in oxygen-limited environments, from the early Earth to present-day expanding hypoxic zones.

Sulfate-reducing microorganisms represent a globally important link between the sulfur and carbon cycles. Recent metagenomic surveys expanded the diversity of microorganisms putatively involved in sulfate reduction underscoring our incomplete understanding of this functional guild. Here, we use genome-centric metatranscriptomics to study the energy metabolism of Acidobacteriota that carry genes for dissimilation of sulfur compounds in a long-term continuous culture running under alternating anoxic and oxic conditions. Differential gene expression analysis reveals the unique metabolic flexibility of a pectin-degrading acidobacterium to switch from sulfate to oxygen reduction when shifting from anoxic to oxic conditions. The combination of facultative anaerobiosis and polysaccharide degradation expands the metabolic versatility among sulfate-reducing microorganisms. Our results highlight that sulfate reduction and aerobic respiration are not mutually exclusive in the same organism, sulfate reducers can mineralize organic polymers, and anaerobic mineralization of complex organic matter is not necessarily a multi-step process involving different microbial guilds but can be bypassed by a single microbial species. Sulfate-reducing microorganisms are common in anoxic environments and represent an important link between the sulfur and carbon cycles. Here, Dyksma & Pester show that microbial sulfate reduction and aerobic respiration are not mutually exclusive in the same organism, sulfate reducers can mineralize organic polymers, and anaerobic mineralization of complex organic matter is not necessarily a multi-step process.

Receptor-interacting protein kinase 3 (RIP3)-regulated production of reactive oxygen species (ROS) positively feeds back on tumour necrosis factor (TNF)-induced necroptosis, a type of programmed necrosis. Glutamine catabolism is known to contribute to RIP3-mediated ROS induction, but the major contributor is unknown. Here, we show that RIP3 activates the pyruvate dehydrogenase complex (PDC, also known as PDH), the rate-limiting enzyme linking glycolysis to aerobic respiration, by directly phosphorylating the PDC E3 subunit (PDC-E3) on T135. Upon activation, PDC enhances aerobic respiration and subsequent mitochondrial ROS production. Unexpectedly, mixed-lineage kinase domain-like (MLKL) is also required for the induction of aerobic respiration, and we further show that it is required for RIP3 translocation to meet mitochondria-localized PDC. Our data uncover a regulation mechanism of PDC activity, show that PDC activation by RIP3 is most likely the major mechanism activated by TNF to increase aerobic respiration and its by-product ROS, and suggest that RIP3-dependent induction of aerobic respiration contributes to pathologies related to oxidative stress. RIP3 regulates mitochondrial metabolism. Yang et al. show that RIP3 activates the pyruvate dehydrogenase complex to enhance aerobic respiration and increase mitochondrial ROS during necroptosis, and MLKL is required for RIP3 translocation to mitochondria.

The atmosphere has recently been recognized as a major source of energy sustaining life. Diverse aerobic bacteria oxidize the three most abundant reduced trace gases in the atmosphere, namely hydrogen (H2), carbon monoxide (CO) and methane (CH4). This Review describes the taxonomic distribution, physiological role and biochemical basis of microbial oxidation of these atmospheric trace gases, as well as the ecological, environmental, medical and astrobiological importance of this process. Most soil bacteria and some archaea can survive by using atmospheric H2 and CO as alternative energy sources, as illustrated through genetic studies on Mycobacterium cells and Streptomyces spores. Certain specialist bacteria can also grow on air alone, as confirmed by the landmark characterization of Methylocapsa gorgona, which grows by simultaneously consuming atmospheric CH4, H2 and CO. Bacteria use high-affinity lineages of metalloenzymes, namely hydrogenases, CO dehydrogenases and methane monooxygenases, to utilize atmospheric trace gases for aerobic respiration and carbon fixation. More broadly, trace gas oxidizers enhance the biodiversity and resilience of soil and marine ecosystems, drive primary productivity in extreme environments such as Antarctic desert soils and perform critical regulatory services by mitigating anthropogenic emissions of greenhouse gases and toxic pollutants.In this Review, Greening and Grinter describe the microorganisms and enzymes that use atmospheric trace gases, including hydrogen, carbon monoxide and methane, during growth and survival. They highlight important ecological and biogeochemical roles for these processes in diverse environments, including ecosystem resilience under changing conditions.

Extracellular electron transfer (EET) describes microbial bioelectrochemical processes in which electrons are transferred from the cytosol to the exterior of the cell 1 . Mineral-respiring bacteria use elaborate haem-based electron transfer mechanisms 2 – 4 but the existence and mechanistic basis of other EETs remain largely unknown. Here we show that the food-borne pathogen Listeria monocytogenes uses a distinctive flavin-based EET mechanism to deliver electrons to iron or an electrode. By performing a forward genetic screen to identify L. monocytogenes mutants with diminished extracellular ferric iron reductase activity, we identified an eight-gene locus that is responsible for EET. This locus encodes a specialized NADH dehydrogenase that segregates EET from aerobic respiration by channelling electrons to a discrete membrane-localized quinone pool. Other proteins facilitate the assembly of an abundant extracellular flavoprotein that, in conjunction with free-molecule flavin shuttles, mediates electron transfer to extracellular acceptors. This system thus establishes a simple electron conduit that is compatible with the single-membrane structure of the Gram-positive cell. Activation of EET supports growth on non-fermentable carbon sources, and an EET mutant exhibited a competitive defect within the mouse gastrointestinal tract. Orthologues of the genes responsible for EET are present in hundreds of species across the Firmicutes phylum, including multiple pathogens and commensal members of the intestinal microbiota, and correlate with EET activity in assayed strains. These findings suggest a greater prevalence of EET-based growth capabilities and establish a previously underappreciated relevance for electrogenic bacteria across diverse environments, including host-associated microbial communities and infectious disease. The Gram-positive Listeria monocytogenes pathogen possesses a distinctive extracellular electron transfer mechanism, which is probably present in numerous ecologically diverse species of the Firmcutes phylum.