ISME Journal最新文献

Long-term climate history can influence rates of soil carbon cycling but the microbial traits underlying these legacy effects are not well understood. Legacies may result if historical climate differences alter the traits of soil microbial communities, particularly those associated with carbon cycling and stress tolerance. However, it is also possible that contemporary conditions can overcome the influence of historical climate, particularly under extreme conditions. Using shotgun metagenomics, we assessed the composition of soil microbial functional genes across a mean annual precipitation gradient that previously showed evidence of strong climate legacies in soil carbon flux and extracellular enzyme activity. Sampling coincided with recovery from a regional, multi-year severe drought, allowing us to document how the strength of climate legacies varied with contemporary conditions. We found increased investment in genes associated with resource cycling with historically higher precipitation across the gradient, particularly in traits related to resource transport and complex carbon degradation. This legacy effect was strongest in seasons with the lowest soil moisture, suggesting that contemporary conditions-particularly, resource stress under water limitation-influences the strength of legacy effects. In contrast, investment in stress tolerance did not vary with historical precipitation, likely due to frequent periodic drought throughout the gradient. Differences in the relative abundance of functional genes explained over half of variation in microbial functional capacity-potential enzyme activity-more so than historical precipitation or current moisture conditions. Together, these results suggest that long-term climate can alter the functional potential of soil microbial communities, leading to legacies in carbon cycling.

The microbial sampling of submarine hydrothermal vents remains challenging, with even fewer studies focused on viruses. Here we report the first isolation of a eukaryotic virus from the Lost City hydrothermal field, by co-culture with the laboratory host Acanthamoeba castellanii. This virus, named pacmanvirus lostcity, is closely related to previously isolated pacmanviruses (strains A23 and S19), clustering in a divergent clade within the long-established family Asfarviridae. Its icosahedral particles are 200 nm in diameter, with an electron-dense core surrounded by an inner membrane. Its genome of 395 708 bp (33% G + C) is predicted to encode 473 proteins. However, besides these standard properties, pacmanvirus lostcity was found associated with a new type of selfish genetic element, 7 kb in length, whose architecture and gene content are reminiscent of those of transpovirons, hitherto specific to the family Mimiviridae. Like previously described transpovirons, this element propagates as an episome within its host virus particles and exhibits partial recombination with its genome. In addition, an unrelated 2 kb long episome was also associated with pacmanvirus lostcity. Together, the transpoviron and the 2 kb episome might participate to exchanges between pacmanviruses and other large DNA virus families. It remains to be elucidated if the presence of these mobile genetic elements is restricted to pacmanviruses or was simply overlooked in other members of the Asfarviridae.

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 wide-spread key life history trait observed across the tree of life. Many plankton species form dormant cells 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 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 6 different time points of the past 6871 ± 140 years, are genetically differentiated and fundamental physiological functions such as growth and photosynthesis had 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.

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.

Sponges largely depend on their symbiotic microbes for their nutrition, health, and survival. This is especially true in high microbial abundance (HMA) sponges, where filtration is usually deprecated in favor of a larger association with prokaryotic symbionts. Sponge-microbiome association is substantially less understood for deep-sea sponges than for shallow water species. This is most unfortunate, since HMA sponges can form massive sponge grounds in the deep sea, where they dominate the ecosystems, driving their biogeochemical cycles. Here, we assess the microbial transcriptional profile of three different deep-sea HMA sponges in four locations of the Cantabrian Sea and compared them to shallow water HMA and LMA (low microbial abundance) sponge species. Our results reveal that the sponge microbiome has converged in a fundamental metabolic role for deep-sea sponges, independent of taxonomic relationships or geographic location, which is shared in broad terms with shallow HMA species. We also observed a large number of redundant microbial members performing the same functions, likely providing stability to the sponge inner ecosystem. A comparison between the community composition of our deep-sea sponges and another 39 species of HMA sponges from deep-sea and shallow habitats, belonging to the same taxonomic orders, suggested strong homogeneity in microbial composition (i.e. weak species-specificity) in deep sea species, which contrasts with that observed in shallow water counterparts. This convergence in microbiome composition and functionality underscores the adaptation to an extremely restrictive environment with the aim of exploiting the available resources.

Photosynthetic cryptophytes are ubiquitous protists that are major participants in the freshwater phytoplankton bloom at the onset of spring. Mortality due to change in environmental conditions and grazing have been recognized as key factors contributing to bloom collapse. In contrast, the role of viral outbreaks as factors terminating phytoplankton blooms remains unknown from freshwaters. Here, we isolated and characterized a cryptophyte virus contributing to the annual collapse of a natural cryptophyte spring bloom population. This viral isolate is also representative for a clade of abundant giant viruses (phylum Nucleocytoviricota) found in freshwaters all over the world.

Viruses are a major control on populations of microbes. Often, their virulence is examined in controlled laboratory conditions. Yet, in nature, environmental conditions lead to changes in host physiology and fitness that may impart both costs and benefits on viral success. Phosphorus (P) is a major abiotic control on the marine cyanobacterium Synechococcus. Some viruses infecting Synechococcus have acquired, from their host, a gene encoding a P substrate binding protein (PstS), thought to improve virus replication under phosphate starvation. Yet, pstS is uncommon among cyanobacterial viruses. Thus, we asked how infections with viruses lacking PstS are affected by P scarcity. We show that the production of infectious virus particles of such viruses is reduced in low P conditions. However, this reduction in progeny is not caused by impaired phage genome replication, thought to be a major sink for cellular phosphate. Instead, transcriptomic analysis showed that under low P conditions, a PstS-lacking cyanophage increased the expression of a specific gene set that included mazG, hli2, and gp43 encoding a pyrophosphatase, a high-light inducible protein and DNA polymerase, respectively. Moreover, several of the upregulated genes were controlled by the host's phoBR two-component system. We hypothesize that recycling and polymerization of nucleotides liberates free phosphate and thus allows viral morphogenesis, albeit at lower rates than when phosphate is replete or when phages encode pstS. Altogether, our data show how phage genomes, lacking obvious P-stress-related genes, have evolved to exploit their host's environmental sensing mechanisms to coordinate their own gene expression in response to resource limitation.