ISME Journal最新文献

Dark carbon fixation (DCF), conducted mainly by chemoautotrophs, contributes greatly to primary production and the global carbon budget. Understanding the response of DCF process to climate warming in coastal wetlands is of great significance for model optimization and climate change prediction. Here, based on a 4-yr field warming experiment (average annual temperature increase of 1.5°C), DCF rates were observed to be significantly inhibited by warming in coastal wetlands (average annual DCF decline of 21.6%, and estimated annual loss of 0.08-1.5 Tg C yr-1 in global coastal marshes), thus causing a positive climate feedback. Under climate warming, chemoautotrophic microbial abundance and biodiversity, which were jointly affected by environmental changes such as soil organic carbon and water content, were recognized as significant drivers directly affecting DCF rates. Metagenomic analysis further revealed that climate warming may alter the pattern of DCF carbon sequestration pathways in coastal wetlands, increasing the relative importance of the 3-hydroxypropionate/4-hydroxybutyrate cycle, whereas the relative importance of the dominant chemoautotrophic carbon fixation pathways (Calvin-Benson-Bassham cycle and W-L pathway) may decrease due to warming stress. Collectively, our work uncovers the feedback mechanism of microbially mediated DCF to climate warming in coastal wetlands, and emphasizes a decrease in carbon sequestration through DCF activities in this globally important ecosystem under a warming climate.

Many bacteria kill competitors using short-range weapons, such as the Type VI secretion system and contact dependent inhibition (CDI). Although these weapons can deliver powerful toxins, they rely on direct contact between attacker and target cells. We hypothesized that movement enables attackers to contact more targets and thus greatly empower their weapons. To explore this, we developed individual-based and continuum models of contact-dependent combat which show that motility greatly improves toxin delivery through two underlying processes. First, genotypic mixing increases the inter-strain contact probability of attacker and sensitive cells. Second, target switching ensures attackers constantly attack new cells, instead of repeatedly hitting the same cell. We test our predictions with the pathogen Pseudomonas aeruginosa, using genetically engineered strains to study the interaction between CDI and twitching motility. As predicted, we find that motility works synergistically with CDI, in some cases increasing weapon efficacy up to 10,000-fold compared with non-motile scenarios. Moreover, we demonstrate that both mixing processes occur using timelapse single-cell microscopy and quantify their relative importance by combining experimental data with our model. Our work shows how bacteria can combine cell movement with contact-based weapons to launch powerful attacks on their competitors.

Inflammatory bowel disease (IBD), including Crohn's disease (CD) and ulcerative colitis (UC), is associated with a loss or an imbalance of host-microorganism interactions. However, such interactions at protein levels remain largely unknown. Here, we applied a depletion-assisted metaproteomics approach to obtain in-depth host-microbiome association networks of IBD, where the core host proteins shifted from those maintaining mucosal homeostasis in controls to those involved in inflammation, proteolysis, and intestinal barrier in IBD. Microbial nodes such as short-chain fatty-acid producer-related host-microbial crosstalk were lost or suppressed by inflammatory proteins in IBD. Guided by protein-protein association networks, we employed proteomics and lipidomics to investigate the effects of UC-related core proteins S100A8, S100A9, and cytokines (IL-1β, IL-6, and TNF-α) on gut bacteria. These proteins suppressed purine nucleotide biosynthesis in stool-derived in vitro communities, which was also reduced in IBD stool samples. Single species study revealed that S100A8, S100A9, and cytokines can synergistically or antagonistically alter gut bacteria intracellular and secreted proteome, with combined S100A8 and S100A9 potently inhibiting beneficial Bifidobacterium adolescentis. Furthermore, these inflammatory proteins only altered the extracellular but not intracellular proteins of Ruminococcus gnavus. Generally, S100A8 induced more significant bacterial proteome changes than S100A9, IL-1β, IL-6, and TNF-α but gut bacteria degrade significantly more S100A8 than S100A9 in the presence of both proteins. Among the investigated species, distinct lipid alterations were only observed in Bacteroides vulgatus treated with combined S100A8, S100A9, and cytokines. These results provided a valuable resource of inflammatory protein-centric host-microbial molecular interactions.

Probiotics have gained significant attention as a potential strategy to improve health by modulating host-microbe interactions, particularly in situations where the normal microbiota has been disrupted. However, evidence regarding their efficacy has been inconsistent, with considerable interindividual variability in response. We aimed to explore whether a common genetic variant that affects the production of mucosal α(1,2)-fucosylated glycans, present in around 20% of the population, could explain the observed interpersonal differences in the persistence of commonly used probiotics. Using a mouse model with varying α(1,2)-fucosylated glycans secretion (Fut2WT or Fut2KO), we examined the abundance and persistence of Bifidobacterium strains (infantis, breve, and bifidum). We observed significant differences in baseline gut microbiota characteristics between Fut2WT and Fut2KO littermates, with Fut2WT mice exhibiting enrichment of species able to utilize α(1,2)-fucosylated glycans. Following antibiotic exposure, only Fut2WT animals showed persistent engraftment of Bifidobacterium infantis, a strain able to internalize α(1,2)-fucosylated glycans, whereas B. breve and B. bifidum, which cannot internalize α(1,2)-fucosylated glycans, did not exhibit this difference. In mice with an intact commensal microbiota, the relationship between secretor status and B. infantis persistence was reversed, with Fut2KO animals showing greater persistence compared to Fut2WT. Our findings suggest that the interplay between a common genetic variation and antibiotic exposure plays a crucial role in determining the dynamics of B. infantis in the recipient gut, which could potentially contribute to the observed variation in response to this commonly used probiotic species.

Prior work has shown a positive scaling relationship between vertebrate body size, human height, and gut microbiome alpha diversity. This observation mirrors commonly observed species area relationships (SARs) in many other ecosystems. Here, we expand these observations to several large datasets, showing that this size-diversity scaling relationship is independent of relevant covariates, like diet, body mass index, age, sex, bowel movement frequency, antibiotic usage, and cardiometabolic health markers. Island biogeography theory (IBT), which predicts that larger islands tend to harbor greater species diversity through neutral demographic processes, provides a simple mechanism for positive SARs. Using a gut-adapted IBT model, we demonstrated that increasing the length of a flow-through ecosystem led to increased species diversity, closely matching our empirical observations. We delve into the possible clinical implications of these SARs in the American Gut cohort. Consistent with prior observations that lower alpha diversity is a risk factor for Clostridioides difficile infection (CDI), we found that individuals who reported a history of CDI were shorter than those who did not and that this relationship was mediated by alpha diversity. We observed that vegetable consumption had a much stronger association with CDI history, which was also partially mediated by alpha diversity. In summary, we find that the positive scaling observed between body size and gut alpha diversity can be plausibly explained by a gut-adapted IBT model, may be related to CDI risk, and vegetable intake appears to independently mitigate this risk, although additional work is needed to validate the potential disease risk implications.

As unicellular predators, ciliates engage in close associations with diverse microbes, laying the foundation for the establishment of endosymbiosis. Originally heterotrophic, ciliates demonstrate the ability to acquire phototrophy by phagocytizing unicellular algae or by sequestering algal plastids. This adaptation enables them to gain photosynthate and develop resistance to unfavorable environmental conditions. The integration of acquired phototrophy with intrinsic phagotrophy results in a trophic mode known as mixotrophy. Additionally, ciliates can harbor thousands of bacteria in various intracellular regions, including the cytoplasm and nucleus, exhibiting species specificity. Under prolonged and specific selective pressure within hosts, bacterial endosymbionts evolve unique lifestyles and undergo particular reductions in metabolic activities. Investigating the research advancements in various endosymbiotic cases within ciliates will contribute to elucidate patterns in cellular interaction and unravel the evolutionary origins of complex traits.

Giant viruses (GVs) significantly regulate the ecological dynamics of diverse ecosystems. Although metagenomics has expanded our understanding of their diversity and ecological roles played in marine environments, little is known about GVs of freshwater ecosystems. Most previous studies have employed short-read sequencing and therefore resulted in fragmented genomes, hampering accurate assessment of genetic diversity. We sought to bridge this knowledge gap and overcome previous technical limitations. We subjected spatiotemporal (2 depths × 12 months) samples from Lake Biwa to metagenome-assembled genome reconstruction enhanced by long-read metagenomics. This yielded 293 GV metagenome-assembled genomes. Of these, 285 included previously unknown species in five orders of nucleocytoviruses and the first representatives of freshwater mirusviruses, which exhibited marked divergence from marine-derived lineages. The good performance of our long-read metagenomic assembly was demonstrated by the detection of 42 (14.3%) genomes composed of single contigs with completeness values >90%. GVs were partitioned across water depths, with most species specific to either the sunlit epilimnion or the dark hypolimnion. Epilimnion-specific members tended to be transient and exhibit short and intense abundance peaks, in line with the fact that they regulate the surface algal blooms. During the spring bloom, mirusviruses and members of three nucleocytovirus families were among the most abundant viruses. In contrast, hypolimnion-specific ones, including a mirusvirus genome, were typically more persistent in the hypolimnion throughout the water-stratified period, suggesting that they infect hosts specific to the hypolimnion and play previously unexplored ecological roles in dark water microbial ecosystems.

Microbial rhodopsins are prevalent in many cyanobacterial groups as a light-energy-harvesting system in addition to the photosynthetic system. It has been suggested that this dual system allows efficient capture of sunlight energy using complementary ranges of absorption wavelengths. However, the diversity of cyanobacterial rhodopsins, particularly in accumulated metagenomic data, remains underexplored. Here, we used a metagenomic mining approach, which led to the identification of a novel rhodopsin clade unique to cyanobacteria, cyanorhodopsin-II (CyR-II). CyR-IIs function as light-driven outward H+ pumps. CyR-IIs, together with previously identified cyanorhodopsins (CyRs) and cyanobacterial halorhodopsins (CyHRs), constitute cyanobacterial ion-pumping rhodopsins (CyipRs), a phylogenetically distinct family of rhodopsins. The CyR-II clade is further divided into two subclades, YCyR-II and GCyR-II, based on their specific absorption wavelength. YCyR-II absorbed yellow light (λmax = 570 nm), whereas GCyR-II absorbed green light (λmax = 550 nm). X-ray crystallography and mutational analysis revealed that the difference in absorption wavelengths is attributable to slight changes in the side chain structure near the retinal chromophore. The evolutionary trajectory of cyanobacterial rhodopsins suggests that the function and light-absorbing range of these rhodopsins have been adapted to a wide range of habitats with variable light and environmental conditions. Collectively, these findings shed light on the importance of rhodopsins in the evolution and environmental adaptation of cyanobacteria.

Physiological responses of soil microorganisms to global warming are important for soil ecosystem function and the terrestrial carbon cycle. Here, we investigate the effects of weeks, years, and decades of soil warming across seasons and time on the microbial protein biosynthesis machineries (i.e. ribosomes), the most abundant cellular macromolecular complexes, using RNA:DNA and RNA:MBC (microbial biomass carbon) ratios as proxies for cellular ribosome contents. We compared warmed soils and non-warmed controls of 15 replicated subarctic grassland and forest soil temperature gradients subject to natural geothermal warming. RNA:DNA ratios tended to be lower in the warmed soils during summer and autumn, independent of warming duration (6 weeks, 8-14 years, and > 50 years), warming intensity (+3°C, +6°C, and +9°C), and ecosystem type. With increasing temperatures, RNA:MBC ratios were also decreasing. Additionally, seasonal RNA:DNA ratios of the consecutively sampled forest showed the same temperature-driven pattern. This suggests that subarctic soil microorganisms are depleted of ribosomes under warm conditions and the lack of consistent relationships with other physicochemical parameters besides temperature further suggests temperature as key driver. Furthermore, in incubation experiments, we measured significantly higher CO2 emission rates per unit of RNA from short- and long-term warmed soils compared to non-warmed controls. In conclusion, ribosome reduction may represent a widespread microbial physiological response to warming that offers a selective advantage at higher temperatures, as energy and matter can be reallocated from ribosome synthesis to other processes including substrate uptake and turnover. This way, ribosome reduction could have a substantial effect on soil carbon dynamics.