ISME Journal最新文献

Dinoflagellates are an abundant and diverse group of protists that inhabit aquatic environments worldwide. They are characterized by numerous unique cellular and molecular traits, and have adapted to an unusually broad range of life strategies, including phototrophy, heterotrophy, parasitism, and all combinations of these. For most microbial groups, transitions from marine to freshwater environments are relatively rare, as changes in salinity are thought to lead to significant osmotic challenges that are difficult for the cell to overcome. Recent work has shown that dinoflagellates have overcome these challenges relatively often in evolutionary time, but because this is mostly based on single gene trees with low overall support, many of the relationships between freshwater and marine groups remain unresolved. Normally, phylogenomics could clarify such conclusions, but despite the recent surge in data, virtually no freshwater dinoflagellates have been characterized at the genome-wide level. Here, we generated 30 transcriptomes from cultures and single cells collected from freshwater environments to infer a robustly supported phylogenomic tree from 217 conserved genes, resolving at least seven transitions to freshwater in dinoflagellates. Mapping the distribution of ASVs from freshwater environmental samples onto this tree confirms these groups and identifies additional lineages where freshwater dinoflagellates likely remain unsampled. We also sampled two species of Durinskia, a genus of "dinotoms" with both marine and freshwater lineages containing Nitzschia-derived tertiary plastids. Ribosomal RNA phylogenies show that the host cells are closely related, but their endosymbionts are likely descended from two distantly-related freshwater Nitzschia species that were acquired in parallel and relatively recently.

Pelagic calcifying protists such as coccolithophores and foraminifera represent an important microbial component of the marine carbon cycle. Although their calcitic shells are preserved in oceanic sediments over millennia, their resilience in the future decades is uncertain. We review current literature describing the response of calcifying protists to ocean acidification and temperature warming. We examine these key ecological and biogeochemical processes through the cellular perspective, exploring the physiological, metabolic, and molecular responses of calcifying protists. Ocean acidification is a chemical process that takes place in the seawater outside the cell, whereas protists calcify inside a modified cellular microenvironment. The function of these calcification compartments depends on cellular response to ocean acidification, such as maintaining pH homeostasis. The response of calcifying protists to ocean acidification and temperature warming is species-specific, with no unifying trends but rather a range of sensitivity levels. Coccolithophores and foraminifera display physiological sensitivity that may hamper their ecological success in comparison to non-calcifying species. Yet, certain species may be more adaptable, especially when comparing to highly vulnerable calcifying molluscs as pteropods. As the molecular machinery mediating cellular calcification is not fully resolved, as well as the functional role of the calcitic shell, our ability to predict the fate of calcifying microorganisms in a warmer, more acidic ocean is limited. We propose the urgent need to expand the study of these model systems by advancing cell biology approaches, to better understand the impact of climate change on microbial food webs in the ocean.

The diffusible toxin ColIb produced by Salmonella enterica serovar Typhimurium SL1344 is a potent inhibitor of Escherichia coli growth. To identify and parameterize metabolic cross-feeding in states of competition, we established defined communities in which E. coli was the only species able to access a sole carbon source, lactose. Although ColIb was predicted to undermine cross-feeding by killing the lactose-converting E. coli, S. enterica populations thrived in co-culture. We discovered that ColIb caused the release of active β-galactosidase from E. coli cells, which induced galactose uptake by S. enterica. Although iron limitation stimulates ColIb production and makes E. coli more sensitive to the toxin, ColIb killing in iron-limited conditions did not enhance iron acquisition or siderophore scavenging by S. enterica. Also unexpected was the rapid rate at which resistance to ColIb evolved in E. coli through spontaneous mutation of the ColIb receptor gene cirA or horizontal acquisition of the S. enterica colicin immunity gene imm. Mathematical modelling effectively predicted the growth kinetics of E. coli and S. enterica populations, revealing a tractable system in which ColIb can shrink a competitor population while simultaneously amplifying the metabolic contributions of the suppressed population.

The gut microbiome plays a crucial role in human health, and certain bacterial species, such as Faecalibacterium prausnitzii, are particularly beneficial. This study conducted a comprehensive investigation of prebiotic compounds that showed potential for specifically promoting beneficial gut bacteria. Using in vitro fecal cultures and a human intervention study, we identified maltobionic acid and lactobionic acid as compounds that specifically promoted Faecalibacterium growth both in vitro and in vivo without significantly affecting Bifidobacterium, which is typically increased by traditional prebiotics. In a human intervention study (n = 27), a significant increase was observed in Faecalibacterium abundance following maltobionic acid supplementation, with effectiveness correlating with the initial Parabacteroides abundance. Mechanistic investigations revealed a cross-feeding pathway between gut bacteria. In this pathway, Parabacteroides species converted the gluconic acid moiety of maltobionic and lactobionic acids to glucuronic acid, which was then preferentially utilized by Faecalibacterium. These findings suggest that gluconic acid-containing oligosaccharides are promising prebiotics for the targeted enhancement of beneficial Faecalibacterium and underscore the importance of microbial interactions in prebiotic research, offering new avenues for personalized microbiome modulation strategies.

Members of Methylotenera are signature denitrifiers and methylotrophs commonly found together with methanotrophic bacteria in lakes and freshwater sediments. Here we show that three distinct Methylotenera ecotypes were abundant in methane-rich groundwaters recharged during the Pleistocene. Just like in surface water biomes, groundwater Methylotenera often co-occurred with methane-oxidizing bacteria, even though they were generally unable to denitrify. One abundant Methylotenera ecotype expressed a pathway for aerobic methane production from methylphosphonate. This phosphate-acquisition strategy was recently found to contribute to methane production in the oligotrophic, oxic upper ocean. Gene organization, phylogeny, and 3D protein structure of the key enzyme, C-P lyase subunit PhnJ, were consistent with a role in phosphate uptake. We conclude that phosphate may be a limiting nutrient in productive, methane-rich aquifers, and that methylphosphonate degradation might contribute to groundwater methane production.

Pantoea agglomerans is one of four Pantoea species reported in the USA to cause bacterial rot of onion bulbs. However, not all P. agglomerans strains are pathogenic to onion. We characterized onion-associated strains of P. agglomerans to elucidate the genetic and genomic signatures of onion-pathogenic P. agglomerans. We collected >300 P. agglomerans strains associated with symptomatic onion plants and bulbs from public culture collections, research laboratories, and a multi-year survey in 11 states in the USA. Combining the 87 genome assemblies with 100 high-quality, public P. agglomerans genome assemblies we identified two well-supported P. agglomerans phylogroups. Strains causing severe symptoms on onion were only identified in Phylogroup II and encoded the HiVir pantaphos biosynthetic cluster, supporting the role of HiVir as a pathogenicity factor. The P. agglomerans HiVir cluster was encoded in two distinct plasmid contexts: 1) as an accessory gene cluster on a conserved P. agglomerans plasmid (pAggl), or 2) on a mosaic cluster of plasmids common among onion strains (pOnion). Analysis of closed genomes revealed that the pOnion plasmids harbored alt genes conferring tolerance to Allium thiosulfinate defensive chemistry and many harbored cop genes conferring resistance to copper. We demonstrated that the pOnion plasmid pCB1C can act as a natively mobilizable pathogenicity plasmid that transforms P. agglomerans Phylogroup I strains, including environmental strains, into virulent pathogens of onion. This work indicates a central role for plasmids and plasmid ecology in mediating P. agglomerans interactions with onion plants, with potential implications for onion bacterial disease management.

Soil bacteria are prolific producers of a myriad of biologically active secondary metabolites. These natural products play key roles in modern society, finding use as anti-cancer agents, as food additives, and as alternatives to chemical pesticides. As for their original role in interbacterial communication, secondary metabolites have been extensively studied under in vitro conditions, revealing many roles including antagonism, effects on motility, niche colonization, signaling, and cellular differentiation. Despite the growing body of knowledge on their mode of action, biosynthesis, and regulation, we still do not fully understand the role of secondary metabolites on the ecology of the producers and resident communities in situ. Here, we specifically examine the influence of Bacillus subtilis-produced cyclic lipopeptides during the assembly of a bacterial synthetic community, and simultaneously, explore the impact of cyclic lipopeptides on B. subtilis establishment success in a synthetic community propagated in an artificial soil microcosm. We found that surfactin production facilitates B. subtilis establishment success within multiple synthetic communities. Although neither a wild type nor a cyclic lipopeptide non-producer mutant had a major impact on the synthetic community composition over time, both the B. subtilis and the synthetic community metabolomes were altered during co-cultivation. Overall, our work demonstrates the importance of surfactin production in microbial communities, suggesting a broad spectrum of action of this natural product.

Escherichia coli is an increasingly antibiotic-resistant opportunistic pathogen. Few data are available on its ecological and evolutionary dynamics in its primary commensal niche, the vertebrate gut. Using Illumina and/or Nanopore technologies, we sequenced whole genomes of 210 E. coli isolates from 22 stools sampled during a 20-year period from a healthy man (ED) living in Paris, France. All phylogroups, except C, were represented, with a predominance of B2 (34.3%), followed by A and F (19% each) phylogroups. Thirty-five clones were identified based on their haplogroup and pairwise genomic single nucleotide polymorphism distance and classified in three phenotypes according to their abundance and residence time: 25 sub-dominant/transient (52 isolates), five dominant/transient (48 isolates) and five dominant/resident (110 isolates). Four over five dominant/resident clones belonged to B2 and closely related F phylogroups, whereas sub-dominant/transient clones belonged mainly to B1, A and D phylogroups. The long residence times of B2 clones seemed to be counterbalanced by lower colonization abilities. Clones with larger within-host frequency persisted for longer. By comparing ED strain genomes to a collection of commensal E. coli genomes from 359 French individuals, we identified ED-specific genomic properties including an enrichment in genes involved in a metabolic pathway (mhp cluster) and the presence of a very rare antiviral defense island. The E. coli colonization within the gut microbiota was shaped by both the intrinsic properties of the strain lineages, in particular longer residence of phylogroup B2, and the environmental constraints such as diet or phages.

The collective surface motility and swarming behavior of microbes play a crucial role in the formation of polymicrobial communities, shaping ecosystems as diverse as animal and human microbiota, plant rhizospheres, and various aquatic environments. In the human oral microbiota, T9SS-driven gliding bacteria transport non-motile microbes and bacteriophages as cargo, thereby influencing the spatial organization and structural complexity of these polymicrobial communities. However, the physical rules governing the dispersal of T9SS-driven bacterial swarms are barely understood. Here, we collected time-lapse images, under anaerobic conditions, of developing swarms of a T9SS-driven microbe common to the human oral microbiota. Tracking of swarms revealed that small peripheral flares emerging from a colony develop structures that resemble fireworks displaying a chrysanthemum effect and flower-like patterns that convert to wave-like patterns and which further evolve into scattered microcolonies. Particle-image velocimetry showed density-dependent phase transitions and initial vorticity within these emerging patterns. Numerical simulations demonstrate that these patterns arise due to changes in swarm speed and alignment strength. Our data reveal a strategy used by an anaerobic swarming bacterium to control swarm behavior, resulting in scattered microcolonies distant from the mother colony, thus reducing competition for resources among colony members. This might ensure species survival even if conditions change drastically in one location of the human oral cavity.

Dormancy is a widespread key life history trait observed across the tree of life. Many plankton species form dormant cell stages that accumulate in aquatic sediments and, under anoxic conditions, form chronological records of past species and population dynamics under changing environmental conditions. Here we report on the germination of a microscopic alga, the abundant marine diatom Skeletonema marinoi Sarno et Zigone, that had remained dormant for up to 6871 ± 140 years in anoxic sediments of the Baltic Sea and resumed growth when exposed to oxygen and light. Resurrected diatom strains, representing cohorts from six different time points of the past 6871 ± 140 years, are genetically differentiated, and fundamental physiological functions such as growth and photosynthesis have remained stable through time despite distinct environmental dynamics. Showing that resurrection and full functional recovery, in comparison to 3 ± 2 years of dormancy, is possible after millennial resting, we emphasize the relevance of dormancy and living sediment archives. For the future, sediment archives, together with the resurrection approach, would offer a powerful tool to trace adaptive traits over millennia under distinct climatic conditions and elucidate the underlying mechanisms.