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.
{"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}
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.
{"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}
Kaitlin A Schaal, Pauline Manhes, Gregory J Velicer
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.
{"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}
Eleanor C Arrington, Jonathan Tarn, Veronika Kivenson, Brook L Nunn, Rachel M Liu, Blair G Paul, David L Valentine
Aqueous-soluble hydrocarbons dissolve into the ocean’s interior and structure deep-sea microbial populations influenced by natural oil seeps and spills. n-Pentane is a seawater-soluble, volatile compound abundant in petroleum products and reservoirs and will partially partition to the deep-water column following release from the seafloor. In this study, we explore the ecology and niche partitioning of two free-living Cycloclasticus strains recovered from seawater incubations with n-pentane and distinguish them as an open ocean variant and a seep-proximal variant, each with distinct capabilities for hydrocarbon catabolism. Comparative metagenomic analysis indicates the variant more frequently observed further from natural seeps encodes more general pathways for hydrocarbon consumption, including short-chain alkanes, aromatics, and long-chain alkanes, and also possesses redox versatility in the form of respiratory nitrate reduction and thiosulfate oxidation; in contrast, the seep variant specializes in short-chain alkanes and relies strictly on oxygen as the terminal electron acceptor. Both variants observed in our work were dominant ecotypes of Cycloclasticus observed during the Deepwater Horizon disaster, a conclusion supported by 16S rRNA gene analysis and read-recruitment of sequences collected from the submerged oil plume during active flow. A comparative genomic analysis of Cycloclasticus across various ecosystems suggests distinct strategies for hydrocarbon transformations among each clade. Our findings suggest Cycloclasticus is a versatile and opportunistic consumer of hydrocarbons and may have a greater role in the cycling of sulfur and nitrogen, thus contributing broad ecological impact to various ecosystems globally.
{"title":"Hydrocarbon metabolism and petroleum seepage as ecological and evolutionary drivers for Cycloclasticus","authors":"Eleanor C Arrington, Jonathan Tarn, Veronika Kivenson, Brook L Nunn, Rachel M Liu, Blair G Paul, David L Valentine","doi":"10.1093/ismejo/wrae247","DOIUrl":"https://doi.org/10.1093/ismejo/wrae247","url":null,"abstract":"Aqueous-soluble hydrocarbons dissolve into the ocean’s interior and structure deep-sea microbial populations influenced by natural oil seeps and spills. n-Pentane is a seawater-soluble, volatile compound abundant in petroleum products and reservoirs and will partially partition to the deep-water column following release from the seafloor. In this study, we explore the ecology and niche partitioning of two free-living Cycloclasticus strains recovered from seawater incubations with n-pentane and distinguish them as an open ocean variant and a seep-proximal variant, each with distinct capabilities for hydrocarbon catabolism. Comparative metagenomic analysis indicates the variant more frequently observed further from natural seeps encodes more general pathways for hydrocarbon consumption, including short-chain alkanes, aromatics, and long-chain alkanes, and also possesses redox versatility in the form of respiratory nitrate reduction and thiosulfate oxidation; in contrast, the seep variant specializes in short-chain alkanes and relies strictly on oxygen as the terminal electron acceptor. Both variants observed in our work were dominant ecotypes of Cycloclasticus observed during the Deepwater Horizon disaster, a conclusion supported by 16S rRNA gene analysis and read-recruitment of sequences collected from the submerged oil plume during active flow. A comparative genomic analysis of Cycloclasticus across various ecosystems suggests distinct strategies for hydrocarbon transformations among each clade. Our findings suggest Cycloclasticus is a versatile and opportunistic consumer of hydrocarbons and may have a greater role in the cycling of sulfur and nitrogen, thus contributing broad ecological impact to various ecosystems globally.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"80 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2024-12-18","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142849060","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}
Quorum sensing inhibition is a promising novel approach to control bacterial infections. However, it is not clear whether quorum sensing inhibition will impose selective pressure for the spread of resistance against quorum sensing inhibition in pathogen populations. Previous research tried to answer this question by using synthetic growth media, and this revealed that whether or not resistance will spread completely depends on the environment in which it is studied. Therefore, the spread of resistance should be studied in the environment where it ultimately matters: in vivo during infection of a host. Here, using quorum sensing inhibitor-susceptible and -resistant mimics, we show that resistance to quorum sensing inhibition does not spread in host-associated populations of Vibrio campbellii during up to 35 cycles of infection and transmission if the initial frequency of the resistance is low in the pathogen population, whereas it further increases to 100% if it is already prevalent. However, even in the latter case, the resistance spreads at a slower pace than resistance to antibiotics spreads under the same conditions.
{"title":"Weak selection for resistance to quorum sensing inhibition during multiple host infection cycles","authors":"Qian Yang, Tom Defoirdt","doi":"10.1093/ismejo/wrae251","DOIUrl":"https://doi.org/10.1093/ismejo/wrae251","url":null,"abstract":"Quorum sensing inhibition is a promising novel approach to control bacterial infections. However, it is not clear whether quorum sensing inhibition will impose selective pressure for the spread of resistance against quorum sensing inhibition in pathogen populations. Previous research tried to answer this question by using synthetic growth media, and this revealed that whether or not resistance will spread completely depends on the environment in which it is studied. Therefore, the spread of resistance should be studied in the environment where it ultimately matters: in vivo during infection of a host. Here, using quorum sensing inhibitor-susceptible and -resistant mimics, we show that resistance to quorum sensing inhibition does not spread in host-associated populations of Vibrio campbellii during up to 35 cycles of infection and transmission if the initial frequency of the resistance is low in the pathogen population, whereas it further increases to 100% if it is already prevalent. However, even in the latter case, the resistance spreads at a slower pace than resistance to antibiotics spreads under the same conditions.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"256 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2024-12-17","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142841574","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}
Sophie-Carole Chobert, Morgane Roger-Margueritat, Laura Flandrin, Safa Berraies, Christopher T Lefèvre, Ludovic Pelosi, Ivan Junier, Nelle Varoquaux, Fabien Pierrel, Sophie S Abby
It is currently unclear how Pseudomonadota, a phylum that originated around the time of the Great Oxidation Event, became one of the most abundant and diverse bacterial phyla on Earth, with metabolically versatile members colonizing a wide range of environments with different O2 concentrations. Here, we address this question by studying isoprenoid quinones, which are central components of energy metabolism covering a wide range of redox potentials. We demonstrate that a dynamic repertoire of quinone biosynthetic pathways accompanied the diversification of Pseudomonadota. The low potential menaquinone (MK) was lost in an ancestor of Pseudomonadota while the high potential ubiquinone (UQ) emerged. We show that the O2-dependent and O2-independent UQ pathways were both present in the last common ancestor of Pseudomonadota, and transmitted vertically. The O2-independent pathway has a conserved genetic organization and displays signs of positive regulation by the master regulator “fumarate and nitrate reductase” (FNR), suggesting a conserved role for UQ in anaerobiosis across Pseudomonadota. The O2-independent pathway was lost in some lineages but maintained in others, where it favoured a secondary reacquisition of low potential quinones (MK or rhodoquinone), which promoted diversification towards aerobic facultative and anaerobic metabolisms. Our results support that the ecological success of Pseudomonadota is linked to the acquisition of the largest known repertoire of quinones, which allowed adaptation to oxic niches as O2 levels increased on Earth, and subsequent diversification into anoxic or O2-fluctuating environments.
{"title":"Dynamic quinone repertoire accompanied the diversification of energy metabolism in Pseudomonadota","authors":"Sophie-Carole Chobert, Morgane Roger-Margueritat, Laura Flandrin, Safa Berraies, Christopher T Lefèvre, Ludovic Pelosi, Ivan Junier, Nelle Varoquaux, Fabien Pierrel, Sophie S Abby","doi":"10.1093/ismejo/wrae253","DOIUrl":"https://doi.org/10.1093/ismejo/wrae253","url":null,"abstract":"It is currently unclear how Pseudomonadota, a phylum that originated around the time of the Great Oxidation Event, became one of the most abundant and diverse bacterial phyla on Earth, with metabolically versatile members colonizing a wide range of environments with different O2 concentrations. Here, we address this question by studying isoprenoid quinones, which are central components of energy metabolism covering a wide range of redox potentials. We demonstrate that a dynamic repertoire of quinone biosynthetic pathways accompanied the diversification of Pseudomonadota. The low potential menaquinone (MK) was lost in an ancestor of Pseudomonadota while the high potential ubiquinone (UQ) emerged. We show that the O2-dependent and O2-independent UQ pathways were both present in the last common ancestor of Pseudomonadota, and transmitted vertically. The O2-independent pathway has a conserved genetic organization and displays signs of positive regulation by the master regulator “fumarate and nitrate reductase” (FNR), suggesting a conserved role for UQ in anaerobiosis across Pseudomonadota. The O2-independent pathway was lost in some lineages but maintained in others, where it favoured a secondary reacquisition of low potential quinones (MK or rhodoquinone), which promoted diversification towards aerobic facultative and anaerobic metabolisms. Our results support that the ecological success of Pseudomonadota is linked to the acquisition of the largest known repertoire of quinones, which allowed adaptation to oxic niches as O2 levels increased on Earth, and subsequent diversification into anoxic or O2-fluctuating environments.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"7 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2024-12-17","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142849061","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}
Julianne C Yang, Venu Lagishetty, Ezinne Aja, Nerea Arias-Jayo, Candace Chang, Megan Hauer, William Katzka, Yi Zhou, Farzaneh Sedighian, Carolina Koletic, Fengting Liang, Tien S Dong, Jamilla Situ, Ryan Troutman, Heidi Buri, Shrikant Bhute, Carra A Simpson, Jonathan Braun, Noam Jacob, Jonathan P Jacobs
Fecal microbiota transplantation has been vital for establishing whether host phenotypes can be conferred through the microbiome. However, whether the existing microbial ecology along the mouse gastrointestinal tract can be recapitulated in germ-free mice colonized with stool remains unknown. We first identified microbes and their predicted functions specific to each of six intestinal regions in three cohorts of specific pathogen-free mice spanning two facilities. Of these region-specific microbes, the health-linked genus Akkermansia was consistently enriched in the lumen of the small intestine compared to the colon. Predictive functional modeling on 16S rRNA gene amplicon sequencing data recapitulated in shotgun sequencing data revealed increased microbial central metabolism, lipolytic fermentation, and cross-feeding in the small intestine, whereas butyrate synthesis was colon-enriched. Neuroactive compound metabolism also demonstrated regional specificity, including small intestine-enriched gamma-aminobutyric acid degradation and colon-enriched tryptophan degradation. Specifically, the jejunum and ileum stood out as sites with high predicted metabolic and neuromodulation activity. Differences between luminal and mucosal microbiomes within each site of the gastrointestinal tract were largely facility-specific, though there were a few consistent patterns in microbial metabolism in specific pathogen-free mice. These included luminal enrichment of central metabolism and cross-feeding within both the small intestine and the colon, and mucosal enrichment of butyrate synthesis within the colon. Across three cohorts of germ-free mice colonized with mice or human stool, compositional and functional region specificity were inconsistently reproduced. These results underscore the importance of investigating the spatial variation of the gut microbiome to better understand its impact on host physiology.
{"title":"Biogeographical distribution of gut microbiome composition and function is partially recapitulated by fecal transplantation into germ-free mice","authors":"Julianne C Yang, Venu Lagishetty, Ezinne Aja, Nerea Arias-Jayo, Candace Chang, Megan Hauer, William Katzka, Yi Zhou, Farzaneh Sedighian, Carolina Koletic, Fengting Liang, Tien S Dong, Jamilla Situ, Ryan Troutman, Heidi Buri, Shrikant Bhute, Carra A Simpson, Jonathan Braun, Noam Jacob, Jonathan P Jacobs","doi":"10.1093/ismejo/wrae250","DOIUrl":"https://doi.org/10.1093/ismejo/wrae250","url":null,"abstract":"Fecal microbiota transplantation has been vital for establishing whether host phenotypes can be conferred through the microbiome. However, whether the existing microbial ecology along the mouse gastrointestinal tract can be recapitulated in germ-free mice colonized with stool remains unknown. We first identified microbes and their predicted functions specific to each of six intestinal regions in three cohorts of specific pathogen-free mice spanning two facilities. Of these region-specific microbes, the health-linked genus Akkermansia was consistently enriched in the lumen of the small intestine compared to the colon. Predictive functional modeling on 16S rRNA gene amplicon sequencing data recapitulated in shotgun sequencing data revealed increased microbial central metabolism, lipolytic fermentation, and cross-feeding in the small intestine, whereas butyrate synthesis was colon-enriched. Neuroactive compound metabolism also demonstrated regional specificity, including small intestine-enriched gamma-aminobutyric acid degradation and colon-enriched tryptophan degradation. Specifically, the jejunum and ileum stood out as sites with high predicted metabolic and neuromodulation activity. Differences between luminal and mucosal microbiomes within each site of the gastrointestinal tract were largely facility-specific, though there were a few consistent patterns in microbial metabolism in specific pathogen-free mice. These included luminal enrichment of central metabolism and cross-feeding within both the small intestine and the colon, and mucosal enrichment of butyrate synthesis within the colon. Across three cohorts of germ-free mice colonized with mice or human stool, compositional and functional region specificity were inconsistently reproduced. These results underscore the importance of investigating the spatial variation of the gut microbiome to better understand its impact on host physiology.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"243 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2024-12-16","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142832279","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}
Foundational to establishment and recovery of biocrusts is a mutualistic exchange of carbon for nitrogen between pioneer cyanobacteria, including the widespread Microcoleus vaginatus, and heterotrophic diazotrophs in its “cyanosphere”. In other such mutualisms, nitrogen is transferred as amino acids or ammonium, preventing losses through specialized structures, cell apposition or intracellularity. Yet, in the biocrust symbiosis relative proximity achieved through chemotaxis optimizes the exchange. We posited that further partner specificity may stem from using an unusual nitrogen vehicle, urea. We show that representative mutualist M. vaginatus PCC 9802 possesses genes for urea uptake, two ureolytic systems, and the urea cycle, overexpressing only uptake and the rare urea carboxylase/allophanate hydrolase (uc/ah) when in co-culture with mutualist Massilia sp. METH4. In turn, it overexpresses urea biosynthesis, but neither urease nor urea uptake when in co-culture. On nitrogen-free medium, three cyanosphere isolates release urea in co-culture with M. vaginatus but not in monoculture. Conversely, M. vaginatus PCC 9802 grows on urea down to the low micromolar range. In natural biocrusts, urea is at low and stable concentrations that do not support the growth of most local bacteria, but aggregates of mutualists constitute dynamic microscale urea hotspots, and the cyanobacterium responds chemotactically to urea. The coordinated gene co-regulation, physiology of cultured mutualists, distribution of urea pools in nature, and responses of native microbial populations, all suggest that low-concentration urea is likely the main vehicle for interspecies N transfer, helping attain partner specificity, for which the rare high-affinity uc/ah system of Microcoleus. vaginatus is likely central.
生物簇建立和恢复的基础是先驱蓝藻（包括广泛分布的微oleus vaginatus）与其 "蓝藻圈 "中的异养重氮生物之间以碳换氮的互助交换。在其他此类互生关系中，氮是以氨基酸或铵盐的形式转移的，通过特化结构、细胞附着或细胞内性来防止氮的损失。然而，在生物簇共生中，通过趋化作用实现的相对接近可以优化交换。我们推测，进一步的伙伴特异性可能来自于使用一种不寻常的氮载体--尿素。我们发现，具有代表性的互生菌 M. vaginatus PCC 9802 拥有尿素吸收基因、两个尿素分解系统基因和尿素循环基因，在与互生菌 Massilia sp.反过来，在共培养时，它过度表达尿素生物合成，但既不表达尿素酶，也不表达尿素吸收。在无氮培养基上，三种蓝藻分离物在与 M. vaginatus 共培养时释放尿素，而在单培养时则不释放尿素。相反，M. vaginatus PCC 9802 在低至微摩尔范围的尿素中生长。在自然生物群落中，尿素的浓度较低且稳定，无法支持大多数局部细菌的生长，但互生藻的聚集体构成了动态的微尺度尿素热点，蓝藻对尿素产生化学反应。协调的基因共调、培养的互生菌的生理学、自然界中尿素池的分布以及本地微生物种群的反应都表明，低浓度尿素可能是种间氮转移的主要载体，有助于实现伙伴特异性，而微囊藻罕见的高亲和性尿素/尿素系统可能是这种特异性的核心。
{"title":"Urea-based mutualistic transfer of nitrogen in biological soil crusts","authors":"Ana Mercedes Heredia-Velásquez, Soumyadev Sarkar, Finlay Warsop Thomas, Ariadna Cairó Baza, Ferran Garcia-Pichel","doi":"10.1093/ismejo/wrae246","DOIUrl":"https://doi.org/10.1093/ismejo/wrae246","url":null,"abstract":"Foundational to establishment and recovery of biocrusts is a mutualistic exchange of carbon for nitrogen between pioneer cyanobacteria, including the widespread Microcoleus vaginatus, and heterotrophic diazotrophs in its “cyanosphere”. In other such mutualisms, nitrogen is transferred as amino acids or ammonium, preventing losses through specialized structures, cell apposition or intracellularity. Yet, in the biocrust symbiosis relative proximity achieved through chemotaxis optimizes the exchange. We posited that further partner specificity may stem from using an unusual nitrogen vehicle, urea. We show that representative mutualist M. vaginatus PCC 9802 possesses genes for urea uptake, two ureolytic systems, and the urea cycle, overexpressing only uptake and the rare urea carboxylase/allophanate hydrolase (uc/ah) when in co-culture with mutualist Massilia sp. METH4. In turn, it overexpresses urea biosynthesis, but neither urease nor urea uptake when in co-culture. On nitrogen-free medium, three cyanosphere isolates release urea in co-culture with M. vaginatus but not in monoculture. Conversely, M. vaginatus PCC 9802 grows on urea down to the low micromolar range. In natural biocrusts, urea is at low and stable concentrations that do not support the growth of most local bacteria, but aggregates of mutualists constitute dynamic microscale urea hotspots, and the cyanobacterium responds chemotactically to urea. The coordinated gene co-regulation, physiology of cultured mutualists, distribution of urea pools in nature, and responses of native microbial populations, all suggest that low-concentration urea is likely the main vehicle for interspecies N transfer, helping attain partner specificity, for which the rare high-affinity uc/ah system of Microcoleus. vaginatus is likely central.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"8 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2024-12-14","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142820636","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}
Fatma Gomaa, Daniel R Rogers, Daniel R Utter, Christopher Powers, I-ting Huang, David J Beaudoin, Ying Zhang, Colleen Cavanaugh, Virginia P Edgcomb, Joan M Bernhard
Investigations of the metabolic capabilities of anaerobic protists advances our understanding of the evolution of eukaryotic life on Earth and for uncovering analogous extraterrestrial complex microbial life. Certain species of foraminiferan protists live in environments analogous to early Earth conditions when eukaryotes evolved, including sulfidic, anoxic, and hypoxic sediment porewaters. Foraminifera are known to form symbioses as well as to harbor organelles from other eukaryotes (chloroplasts), possibly bolstering the host’s independence from oxygen. The full extent of foraminiferal physiological capabilities is not fully understood. To date, evidence for foraminiferal anaerobiosis was gleaned from specimens first subjected to stresses associated with removal from in situ conditions. Here, we report comprehensive gene expression analysis of benthic foraminiferal populations preserved in situ on the euxinic (anoxic and sulfidic) bathyal seafloor, thus avoiding environmental alterations associated with sample recovery, including pressure reduction, sunlight exposure, warming, and oxygenation. Metatranscriptomics, metagenome-assembled genomes, and measurements of substrate uptake were used to study the kleptoplastidic foraminifer Nonionella stella inhabiting sulfur-oxidizing bacterial mats of the Santa Barbara Basin, off California. We show N. stella energy generation under dark euxinia is unusual because it orchestrates complex metabolic pathways for ATP production and carbon fixation through the Calvin cycle. These pathways include extended glycolysis, anaerobic fermentation, sulfide oxidation, and the presence of a membrane-bound inorganic pyrophosphatase, an enzyme that hydrolyzes inorganic pyrophosphate to actively pump protons across the mitochondrial membrane.
对厌氧原生生物新陈代谢能力的研究有助于我们了解真核生物在地球上的进化过程，也有助于发现类似的地外复杂微生物生命。某些种类的有孔虫原生生物生活的环境与真核生物进化时的早期地球环境类似，包括硫酸、缺氧和缺氧沉积物孔隙水。已知有孔虫能形成共生体，也能容纳其他真核生物的细胞器（叶绿体），这可能会增强宿主对氧气的独立性。有孔虫的全部生理能力尚未完全清楚。迄今为止，有孔虫厌氧性的证据都是在标本脱离原位条件后首先受到压力时收集到的。在此，我们报告了对原位保存在无氧（缺氧和硫酸）深海海底的底栖有孔虫种群进行的全面基因表达分析，从而避免了与样本回收相关的环境改变，包括压力降低、阳光照射、升温和充氧。我们利用元转录组学、元基因组组装基因组和底物吸收测量来研究栖息在加利福尼亚外海圣巴巴拉盆地硫氧化细菌垫中的有孔虫Nonionella stella。我们的研究表明，N. stella 在黑暗无氧状态下产生能量的方式与众不同，因为它通过卡尔文循环协调了产生 ATP 和碳固定的复杂代谢途径。这些途径包括延长的糖酵解、厌氧发酵、硫化物氧化，以及膜结合无机焦磷酸酶的存在，这种酶能水解无机焦磷酸，以积极泵送质子穿过线粒体膜。
{"title":"Array of metabolic pathways in a kleptoplastidic foraminiferan protist supports chemoautotrophy in dark, euxinic seafloor sediments","authors":"Fatma Gomaa, Daniel R Rogers, Daniel R Utter, Christopher Powers, I-ting Huang, David J Beaudoin, Ying Zhang, Colleen Cavanaugh, Virginia P Edgcomb, Joan M Bernhard","doi":"10.1093/ismejo/wrae248","DOIUrl":"https://doi.org/10.1093/ismejo/wrae248","url":null,"abstract":"Investigations of the metabolic capabilities of anaerobic protists advances our understanding of the evolution of eukaryotic life on Earth and for uncovering analogous extraterrestrial complex microbial life. Certain species of foraminiferan protists live in environments analogous to early Earth conditions when eukaryotes evolved, including sulfidic, anoxic, and hypoxic sediment porewaters. Foraminifera are known to form symbioses as well as to harbor organelles from other eukaryotes (chloroplasts), possibly bolstering the host’s independence from oxygen. The full extent of foraminiferal physiological capabilities is not fully understood. To date, evidence for foraminiferal anaerobiosis was gleaned from specimens first subjected to stresses associated with removal from in situ conditions. Here, we report comprehensive gene expression analysis of benthic foraminiferal populations preserved in situ on the euxinic (anoxic and sulfidic) bathyal seafloor, thus avoiding environmental alterations associated with sample recovery, including pressure reduction, sunlight exposure, warming, and oxygenation. Metatranscriptomics, metagenome-assembled genomes, and measurements of substrate uptake were used to study the kleptoplastidic foraminifer Nonionella stella inhabiting sulfur-oxidizing bacterial mats of the Santa Barbara Basin, off California. We show N. stella energy generation under dark euxinia is unusual because it orchestrates complex metabolic pathways for ATP production and carbon fixation through the Calvin cycle. These pathways include extended glycolysis, anaerobic fermentation, sulfide oxidation, and the presence of a membrane-bound inorganic pyrophosphatase, an enzyme that hydrolyzes inorganic pyrophosphate to actively pump protons across the mitochondrial membrane.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"15 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2024-12-13","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142820637","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}
Anna Krzynowek, Broos Van de Moortel, Nikola Pichler, Isabel Vanoverberghe, Johanna Lapere, Liliana M Jenisch, Daphné Deloof, Wim Thielemans, Koenraad Muylaert, Michiel Dusselier, Dirk Springael, Karoline Faust, Ellen Decaestecker
Microplastic pollution in aquatic environments is a growing global concern. Microplastics, defined as plastic fragments smaller than five millimetres, accumulate in freshwater reservoirs, especially in urban areas, impacting resident biota. This study examined the effects of microplastics on the performance and microbiome of Daphnia, a keystone organism in freshwater ecosystems, through both in situ sampling of freshwater ponds and a controlled 23-day in vitro exposure experiment. Using bacterial 16S ribosomal RNA gene amplicon sequencing and whole-genome shotgun sequencing, we analyzed the microbiome's composition and functional capacity in relation to microplastic pollution levels. Urban ponds contained higher microplastic concentrations in water and sediment than natural ponds, with distinct differences in plastic composition. Bacterioplankton communities defined as bacterial assemblages in the water column, were more diverse and richer than Daphnia-associated microbiomes. Overall, the in situ study showed that the composition of the Daphnia-associated community was influenced by many factors including microplastic levels but also temperature and redox potential. Functional analysis showed increased relative abundances of polyethylene terephthalate degradation enzymes and antibiotic resistance genes in microbiomes from high-microplastic ponds. In the in vitro experiment, the bacterioplankton inoculum source significantly influenced Daphnia survival and microbiome composition. Network analysis identified specific taxa associated with microplastics within the Daphnia microbiome. Our findings highlight that urbanisation leads to higher microplastic and antibiotic resistance gene burdens, influencing host-associated microbiomes through taxonomic shifts, functional enrichment, and survival outcomes, with potential implications for the resilience of aquatic ecosystems.
{"title":"Effects of microplastics on daphnia-associated microbiomes in situ and in vitro","authors":"Anna Krzynowek, Broos Van de Moortel, Nikola Pichler, Isabel Vanoverberghe, Johanna Lapere, Liliana M Jenisch, Daphné Deloof, Wim Thielemans, Koenraad Muylaert, Michiel Dusselier, Dirk Springael, Karoline Faust, Ellen Decaestecker","doi":"10.1093/ismejo/wrae234","DOIUrl":"https://doi.org/10.1093/ismejo/wrae234","url":null,"abstract":"Microplastic pollution in aquatic environments is a growing global concern. Microplastics, defined as plastic fragments smaller than five millimetres, accumulate in freshwater reservoirs, especially in urban areas, impacting resident biota. This study examined the effects of microplastics on the performance and microbiome of Daphnia, a keystone organism in freshwater ecosystems, through both in situ sampling of freshwater ponds and a controlled 23-day in vitro exposure experiment. Using bacterial 16S ribosomal RNA gene amplicon sequencing and whole-genome shotgun sequencing, we analyzed the microbiome's composition and functional capacity in relation to microplastic pollution levels. Urban ponds contained higher microplastic concentrations in water and sediment than natural ponds, with distinct differences in plastic composition. Bacterioplankton communities defined as bacterial assemblages in the water column, were more diverse and richer than Daphnia-associated microbiomes. Overall, the in situ study showed that the composition of the Daphnia-associated community was influenced by many factors including microplastic levels but also temperature and redox potential. Functional analysis showed increased relative abundances of polyethylene terephthalate degradation enzymes and antibiotic resistance genes in microbiomes from high-microplastic ponds. In the in vitro experiment, the bacterioplankton inoculum source significantly influenced Daphnia survival and microbiome composition. Network analysis identified specific taxa associated with microplastics within the Daphnia microbiome. Our findings highlight that urbanisation leads to higher microplastic and antibiotic resistance gene burdens, influencing host-associated microbiomes through taxonomic shifts, functional enrichment, and survival outcomes, with potential implications for the resilience of aquatic ecosystems.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"14 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2024-12-12","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142815872","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}
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