The ISME JournalPub Date : 2025-01-20DOI: 10.1093/ismejo/wraf004
Mathias Middelboe, Sachia J Traving, Daniel Castillo, Panos G Kalatzis, Ronnie N Glud
{"title":"Prophage-encoded chitinase gene supports growth of its bacterial host isolated from deep-sea sediments","authors":"Mathias Middelboe, Sachia J Traving, Daniel Castillo, Panos G Kalatzis, Ronnie N Glud","doi":"10.1093/ismejo/wraf004","DOIUrl":"https://doi.org/10.1093/ismejo/wraf004","url":null,"abstract":"Auxiliary metabolic genes encoded by bacteriophages can influence host metabolic function during infection. In temperate phages, auxiliary metabolic genes may increase host fitness when integrated as prophages into the host genome. However, little is known about the contribution of prophage-encoded auxiliary metabolic genes to host metabolic properties. In this study, we examined a temperate bacteriophage, and its piezotolerant Pseudomonas sp. host obtained from sediment samples collected from the Kermadec Trench at ~10 000 m water depth. Both the phage and host were present throughout the sediment profiles from the surface to 30 cm into the sediment, covering large gradients of environmental conditions. The host and phage each carried one chitinase gene, which differed from each other, suggesting that chitin degradation plays a role in their substrate supply. We demonstrated that prophage-encoded chitinase supported host chitin degradation and growth in the presence of chitin. Furthermore, prophage induction dynamics were strongly substrate-dependent, suggesting that the host controls the lysis-lysogeny switch in response to the presence of chitin, thus optimizing the trade-off between the loss of cells from prophage induction and prophage enhancement of host performance. Overall, the results demonstrate prophage-encoded auxiliary metabolic genes as collaborative goods for their hosts and emphasize the potential role of phage-host interactions in benthic biogeochemical cycling, as well as for the capability of deep-sea bacteria to efficiently adapt and thrive at a wide range of environmental conditions.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"13 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2025-01-20","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142991150","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
The ISME JournalPub Date : 2025-01-09DOI: 10.1093/ismejo/wraf003
Cong Liu, Mayra C Vidal
{"title":"Dispersal promotes stability and persistence of exploited yeast mutualisms","authors":"Cong Liu, Mayra C Vidal","doi":"10.1093/ismejo/wraf003","DOIUrl":"https://doi.org/10.1093/ismejo/wraf003","url":null,"abstract":"Multi-species mutualistic interactions are ubiquitous and essential in nature, yet they face several threats, many of which have been exacerbated in the Anthropocene era. Understanding the factors that drive the stability and persistence of mutualism has become increasingly important in light of global change. Although dispersal is widely recognized as a crucial spatially explicit process in maintaining biodiversity and community structure, knowledge about how the dispersal of mutualists contributes to the persistence of mutualistic systems remains limited. In this study, we used a synthetic mutualism formed by genetically modified budding yeast to investigate the effect of dispersal on the persistence and stability of mutualisms under exploitation. We found that dispersal increased the persistence of exploited mutualisms by 80% compared to the isolated systems. Furthermore, our results showed that dispersal increased local diversity, decreased beta diversity among local communities, and stabilized community structure at the regional scale. Our results indicate that dispersal can allow mutualisms to persist in meta-communities by reintroducing species that are locally competitively excluded by exploiters. With limited dispersal, e.g., due to increased fragmentation of meta-communities, mutualisms might be more prone to breakdown. Taken together, our results highlight the critical role of dispersal in facilitating the persistence of mutualism.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"16 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2025-01-09","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142939659","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
The ISME JournalPub Date : 2025-01-08DOI: 10.1093/ismejo/wraf001
Amanda N Shelton, Feiqiao B Yu, Arthur R Grossman, Devaki Bhaya
{"title":"Abundant and active community members respond to diel cycles in hot spring phototrophic mats","authors":"Amanda N Shelton, Feiqiao B Yu, Arthur R Grossman, Devaki Bhaya","doi":"10.1093/ismejo/wraf001","DOIUrl":"https://doi.org/10.1093/ismejo/wraf001","url":null,"abstract":"Photosynthetic microbial mats in hot springs can provide insights into the diel behaviors of communities in extreme environments. In this habitat, photosynthesis dominates during the day, leading to super-oxic conditions, with a rapid transition to fermentation and anoxia at night. Multiple samples were collected from two springs over several years to generate metagenomic and metatranscriptomic datasets. Metagenome assembled genomes comprised 71 taxa (in 19 different phyla), of which twelve core taxa were present at high abundance in both springs. The eight most active taxa identified by metatranscriptomics were an oxygenic cyanobacterium (Synechococcus sp.), five anoxygenic phototrophs from three different phyla, and two understudied heterotrophs from phylum Armatimonadota. In all eight taxa, a significant fraction of genes exhibited a diel expression pattern although peak timing varied considerably. The two abundant heterotrophs exhibit starkly different peak timing of expression, which we propose is shaped by their metabolic and genomic potential to use carbon sources that become differentially available during the diel cycle. Network analysis revealed pathway expression patterns that had not previously been linked to diel cycles, including ribosome biogenesis and chaperones. This provides a framework for analyzing metabolically coupled communities and the dominant role of the diel cycle.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"31 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2025-01-08","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142937341","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
The ISME JournalPub Date : 2025-01-07DOI: 10.1093/ismejo/wrae260
Camille C Mangin, Karim Benzerara, Marine Bergot, Nicolas Menguy, Béatrice Alonso, Stéphanie Fouteau, Raphaël Méheust, Daniel Chevrier, Christian Godon, Elsa Turrini, Neha Mehta, Arnaud Duverger, Cynthia Travert, Vincent Busigny, Elodie Duprat, Romain Bolzoni, Corinne Cruaud, Eric Viollier, Didier Jézéquel, David Vallenet, Christopher T Lefèvre, Caroline L Monteil
{"title":"Magnetotactic bacteria from diverse Pseudomonadota families biomineralize intracellular Ca-carbonate","authors":"Camille C Mangin, Karim Benzerara, Marine Bergot, Nicolas Menguy, Béatrice Alonso, Stéphanie Fouteau, Raphaël Méheust, Daniel Chevrier, Christian Godon, Elsa Turrini, Neha Mehta, Arnaud Duverger, Cynthia Travert, Vincent Busigny, Elodie Duprat, Romain Bolzoni, Corinne Cruaud, Eric Viollier, Didier Jézéquel, David Vallenet, Christopher T Lefèvre, Caroline L Monteil","doi":"10.1093/ismejo/wrae260","DOIUrl":"https://doi.org/10.1093/ismejo/wrae260","url":null,"abstract":"Intracellular calcium carbonate formation has long been associated with a single genus of giant Gammaproteobacteria, Achromatium. However, this biomineralization has recently received increasing attention after being observed in photosynthetic Cyanobacteriota and in two families of magnetotactic bacteria affiliated with the Alphaproteobacteria. In the latter group, bacteria form not only intracellular amorphous calcium carbonates into large inclusions that are refringent under the light microscope, but also intracellular ferrimagnetic crystals into organelles called magnetosomes. Here new observations suggest that magnetotactic bacteria previously identified in the sediments and water column of Lake Pavin (France) were only a small fraction of the diversity of bacteria producing intracellular amorphous calcium carbonates. To explore this diversity further, we conducted a comprehensive investigation of magnetotactic populations with refractive granules using a combination of environmental microbiology, genomic and mineralogy approaches on cells sorted by micromanipulation. Several species belonging to divergent genera of two Pseudomonadota classes were identified and characterized. Scanning transmission electron microscopy coupled with energy-dispersive X-ray spectrometry support that all these species indeed form intracellular amorphous calcium carbonates. Cryo soft X-ray tomography experiments conducted on ice-vitrified cells, enabled 3D investigation of inclusions volume, which was found to occupy 44 – 68% of the cell volume. Metabolic network modeling highlighted different metabolic abilities of Alpha- and Gammaproteobacteria, including methylotrophy and CO2 fixation via the reverse Krebs cycle or the Calvin-Benson-Bassham cycle. Overall, this study strengthens a convergent evolution scenario for intracellular carbonatogenesis in Bacteria, and further supports that it is promoted by the fixation of CO2 in anoxic environments.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"30 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2025-01-07","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142935980","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Polymerization of dietary fructans differentially affects interactions among intestinal microbiota of colitis mice","authors":"Yaqin Xiao, Qianyun Zhao, Dawei Ni, Xiaoqi Zhang, Wei Hao, Qin Yuan, Wei Xu, Wanmeng Mu, Dingtao Wu, Xu Wu, Shengpeng Wang","doi":"10.1093/ismejo/wrae262","DOIUrl":"https://doi.org/10.1093/ismejo/wrae262","url":null,"abstract":"The intestinal microbiota plays a critical role in maintaining human health and can be modulated by dietary interventions and lifestyle choices. Fructans, a dietary carbohydrate, are selectively utilized by the intestinal microbiota to confer health benefits. However, the specific effects of different fructan types on microbial changes and functions remain incompletely understood. Here, we investigated how the intestinal microbiota responds to fructans with varying degrees of polymerization in the context of gut dysbiosis. Both low molecular weight fructo-oligosaccharides and high molecular weight levan suppressed intestinal inflammation in a colitis mouse model, mitigating intestinal fibrosis and dysbiosis. Although both the effects of fructo-oligosaccharides and levan are microbiota-dependent, distinct modulation patterns of the intestinal microbiota were observed based on the molecular weight of the fructans. Levan had a more pronounced and persistent impact on gut microbiota compared to fructo-oligosaccharides. Levan particularly promoted the abundance of Dubosiella newyorkensis, which exhibited preventive effects against colitis. Our findings highlight the importance of polymerization levels of dietary fructans in microbiota alterations and identify Dubosiella newyorkensis as a potential probiotic for treating inflammatory diseases.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"1 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2025-01-02","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142917183","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
The ISME JournalPub Date : 2025-01-02DOI: 10.1093/ismejo/wrae258
Kat Pick, Lauren Stadel, Tracy L Raivio
{"title":"Escherichia coli phage-inducible chromosomal island aids helper phage replication and represses the LEE pathogenicity island","authors":"Kat Pick, Lauren Stadel, Tracy L Raivio","doi":"10.1093/ismejo/wrae258","DOIUrl":"https://doi.org/10.1093/ismejo/wrae258","url":null,"abstract":"In this study, we identify and characterize a novel phage-inducible chromosomal island found in commensal Escherichia coli MP1. This novel element, EcCIMP1, is induced and mobilized by the temperate helper phage vB_EcoP_Kapi1. EcCIMP1 contributes to superinfection immunity against its helper phage, impacting bacterial competition outcomes. Genetic analysis of EcCIMP1 led us to uncover a putative transcriptional repressor, which silences virulence gene expression in the murine pathogen Citrobacter rodentium. We also found a putative excisionase encoded by EcCIMP1 which paradoxically does not promote excision of EcCIMP1, but rather supports excision of the helper phage. Another putative excisionase encoded by a presumed integrative conjugative element can also support excision of vB_EcoP_Kapi1, demonstrating crosstalk between excisionases from multiple classes of mobile genetic elements within the same cell. Although phylogenetically distant from other characterized phage-inducible chromosomal islands, EcCIMP1 and EcCIMP1-like elements are prevalent in both pathogenic and commensal isolates of Escherchia coli from around the world, underscoring the importance of characterizing these abundant genetic elements.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"28 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2025-01-02","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142917578","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
The ISME JournalPub Date : 2024-12-23DOI: 10.1093/ismejo/wrae256
Dina Mant, Tomer Orevi, Nadav Kashtan
{"title":"Impact of micro-habitat fragmentation on microbial population growth dynamics","authors":"Dina Mant, Tomer Orevi, Nadav Kashtan","doi":"10.1093/ismejo/wrae256","DOIUrl":"https://doi.org/10.1093/ismejo/wrae256","url":null,"abstract":"Microbial communities thrive in virtually every habitat on Earth and are essential to the function of diverse ecosystems. Most microbial habitats are not spatially continuous and well-mixed, but rather composed, at the microscale, of many isolated or semi-isolated local patches of different sizes, resulting in partitioning of microbial populations into discrete local populations. The impact of this spatial fragmentation on population dynamics is not well-understood. Here, we study how such variably sized micro-habitat patches affect the growth dynamics of clonal microbial populations and how dynamics in individual patches dictate those of the metapopulation. To investigate this, we developed the μ-SPLASH, an ecology-on-a-chip platform, enabling the culture of microbes in microscopic landscapes comprised of thousands of microdroplets, with a wide range of sizes. Using the μ-SPLASH, we cultured the model bacteria E. coli and based on time-lapse microscopy, analyzed the population dynamics within thousands of individual droplets. Our results reveal that growth curves substantially vary with droplet size. Although growth rates generally increase with drop size, reproductive success and the time to approach carrying capacity, display non-monotonic patterns. Combining μ-SPLASH experiments with computational modeling, we show that these patterns result from both stochastic and deterministic processes, and demonstrate the roles of initial population density, patchiness, and patch size distribution in dictating the local and metapopulation dynamics. This study reveals basic principles that elucidate the effects of habitat fragmentation and population partitioning on microbial population dynamics. These insights deepen our understanding of natural microbial communities and have significant implications for microbiome engineering.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"32 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2024-12-23","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142874344","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Diversification of single-cell growth dynamics under starvation influences subsequent reproduction in a clonal bacterial population","authors":"Sotaro Takano, Miki Umetani, Hidenori Nakaoka, Ryo Miyazaki","doi":"10.1093/ismejo/wrae257","DOIUrl":"https://doi.org/10.1093/ismejo/wrae257","url":null,"abstract":"Most of the microbes in nature infrequently receive nutrients and are thus in slow- or non-growing states. How quickly they can resume their growth upon an influx of new resources is crucial to occupy environmental niches. Isogenic microbial populations are known to harbor only a fraction of cells with rapid growth resumption, yet little is known about the physiological characteristics of those cells and their emergence in the population. Here, we tracked growth of individual Escherichia coli cells in populations under fluctuating nutrient conditions. We found that shifting from high- to low-nutrient conditions caused stalling of cell growth with few cells continuing to divide extremely slowly, a process which was dependent on lipid turnover. Resuming high-nutrient inflow after low-nutrient conditions resulted in cells resuming growth and division, but with different lag times and leading to varying progeny. The history of cell growth during low-nutrient but not high-nutrient conditions was determinant for resumption of growth, which cellular genealogy analysis suggested to originate from inherited physiological differences. Our results demonstrate that cellular growth dynamics become diverse by nutrient limitations, under which a fraction of cells experienced a particular growth history can reproduce progeny with new resources in the future.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"125 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2024-12-23","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142874208","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
The ISME JournalPub Date : 2024-12-23DOI: 10.1093/ismejo/wrae255
Kaitlin A Schaal, Pauline Manhes, Gregory J Velicer
{"title":"Ecological histories govern social exploitation by microorganisms","authors":"Kaitlin A Schaal, Pauline Manhes, Gregory J Velicer","doi":"10.1093/ismejo/wrae255","DOIUrl":"https://doi.org/10.1093/ismejo/wrae255","url":null,"abstract":"Exploitation is a common feature of social interactions, which can be modified by ecological context. Here we investigate effects of ecological history on exploitation phenotypes in bacteria. In experiments with the bacterium Myxococcus xanthus, prior resource levels of different genotypes interacting during cooperative multicellular development were found to regulate social fitness, including whether cheating occurs. Responses of developmental spore production to experimental manipulation of resource-level histories differed between interacting cooperators and cheaters, and relative fitness advantages gained by cheating after high-resource growth were generally reduced or absent if one or both parties experienced low-resource growth. Low-resource growth also eliminated exploitation in some pairwise mixes of cooperative natural isolates that occurs when both strains have grown under resource abundance. Our results contrast with previous experiments in which cooperator fitness correlated positively with concurrent resource level and suggest that resource-level variation may be important in regulating whether exploitation of cooperators occurs in a natural context.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"37 5 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2024-12-23","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142874206","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
The ISME JournalPub Date : 2024-12-21DOI: 10.1093/ismejo/wrae259
Zhiying Lu, Elizabeth Entwistle, Matthew D Kuhl, Alexander R Durrant, Marcelo Malisano Barreto Filho, Anuradha Goswami, J Jeffrey Morris
{"title":"Coevolution of marine phytoplankton and Alteromonas bacteria in response to pCO2 and co-culture","authors":"Zhiying Lu, Elizabeth Entwistle, Matthew D Kuhl, Alexander R Durrant, Marcelo Malisano Barreto Filho, Anuradha Goswami, J Jeffrey Morris","doi":"10.1093/ismejo/wrae259","DOIUrl":"https://doi.org/10.1093/ismejo/wrae259","url":null,"abstract":"As a result of human activity, Earth’s atmosphere and climate are changing at an unprecedented pace. Models based on short-term experiments predict major changes will occur in marine phytoplankton communities in the future ocean, but rarely consider how evolution or interactions with other microbes may influence these changes. Here we experimentally evolved several phytoplankton in co-culture with a heterotrophic bacterium, Alteromonas sp. EZ55, under either present-day or predicted future pCO2 conditions. Growth rates of phytoplankton generally increased over time under both conditions, but only Thalassiosira oceanica had evidence of a growth rate trade-off in the ancestral environment after evolution at elevated pCO2. The growth defects observed in ancestral Prochlorococcus cultures at elevated pCO2 and in axenic culture were diminished after evolution, possibly due to regulatory mutations in antioxidant genes. Except for Prochlorococcus, mutational profiles suggested phytoplankton experienced primarily purifying selection, but most Alteromonas lineages showed evidence of directional selection, where evolution appeared to favor a metabolic switch between growth on small organic acids with cyanobacteria versus catabolism of more complex carbon substrates with eukaryotic phytoplankton. Evolved Alteromonas were also poorer “helpers” for Prochlorococcus, consistent with that interaction being a competitive Black Queen process rather than a true mutualism. This work provides new insights on how phytoplankton will respond to increased pCO2 and on the evolutionary mechanisms governing phytoplankton:bacteria interactions. It also clearly demonstrates that both evolution and interspecies interactions must be considered to predict future marine biogeochemistry.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"43 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2024-12-21","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142879852","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}