Elizabeth C Cooney, Brian S Leander, Patrick J Keeling
Free-living core dinoflagellates are commonly infected by members of two parasitic clades that are themselves closely related to dinoflagellates, the marine alveolates and perkinsids. These parasites are abundant and ecologically important, but most species have been difficult to observe directly or cultivate, so our knowledge of them is usually restricted to environmental 18S rRNA gene sequences, and genome-scale molecular data are not available for most species. Here, we report numerous syndinian parasites and one parasite that is sister to all known perkinsids from isolated single cells of diverse, free-living dinoflagellates. Of the 14 infected host cells collected, only five were noticeably infected via light microscopy at the time of collection. Single-cell transcriptome sequencing yielded relatively high transcriptomic coverage for parasites as well as their hosts. Host and parasite homologs were distinguished phylogenetically allowing us to infer a robust phylogenomic tree based on 198 genes. The tree showed one parasite belongs to an undescribed lineage that is sister to perkinsids, whereas the remainder are members of the syndinian clade. Close relatives of all these parasites have been observed in 18S rRNA gene surveys, but until now none had been linked to a specific host. These findings illustrate the efficacy of single-cell isolation and transcriptome sequencing as a strategy for gaining deeper insights into the evolutionary history and host relationships of hidden single-celled parasites.
{"title":"Hidden syndinian and perkinsid infections in dinoflagellate hosts revealed by single-cell transcriptomics","authors":"Elizabeth C Cooney, Brian S Leander, Patrick J Keeling","doi":"10.1093/ismejo/wrae188","DOIUrl":"https://doi.org/10.1093/ismejo/wrae188","url":null,"abstract":"Free-living core dinoflagellates are commonly infected by members of two parasitic clades that are themselves closely related to dinoflagellates, the marine alveolates and perkinsids. These parasites are abundant and ecologically important, but most species have been difficult to observe directly or cultivate, so our knowledge of them is usually restricted to environmental 18S rRNA gene sequences, and genome-scale molecular data are not available for most species. Here, we report numerous syndinian parasites and one parasite that is sister to all known perkinsids from isolated single cells of diverse, free-living dinoflagellates. Of the 14 infected host cells collected, only five were noticeably infected via light microscopy at the time of collection. Single-cell transcriptome sequencing yielded relatively high transcriptomic coverage for parasites as well as their hosts. Host and parasite homologs were distinguished phylogenetically allowing us to infer a robust phylogenomic tree based on 198 genes. The tree showed one parasite belongs to an undescribed lineage that is sister to perkinsids, whereas the remainder are members of the syndinian clade. Close relatives of all these parasites have been observed in 18S rRNA gene surveys, but until now none had been linked to a specific host. These findings illustrate the efficacy of single-cell isolation and transcriptome sequencing as a strategy for gaining deeper insights into the evolutionary history and host relationships of hidden single-celled parasites.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"3 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2024-09-26","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142325509","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}
Hugo Sentenac, Dirk S Schmeller, Solène Caubet, Adélaïde Carsin, Rémi Guillet, Jessica Ferriol, Joséphine Leflaive, Adeline Loyau
Emerging infectious diseases threaten biodiversity and human health. Many emerging pathogens have aquatic life stages and all immersed substrates have biofilms on their surface, i.e., communities of microorganisms producing a gelatinous matrix. However, the outcome of the interactions between environmental biofilms and pathogens is poorly understood. Here we demonstrate that biofilms reduce the survival of the most impactful pathogen for vertebrate diversity, the invasive chytrid fungus Batrachochytrium dendrobatidis. Effects on its zoospores varied with biofilm composition in controlled settings and biofilm compositional variation also coincided with divergent impacts of chytridiomycosis on amphibian populations in nature. Our results suggest that biofilms form a biotic component of ecosystem resistance to Batrachochytrium dendrobatidis by reducing environmental transmission, and that they could be used to develop nature-based technologies to limit the impacts and spread of this invasive chytrid fungus. Our study warrants further research into the interactions between environmental biofilms and pathogenic and/or invasive micro-organisms.
{"title":"Biofilms inactivate the free-living stage of Batrachochytrium dendrobatidis, the most destructive pathogen for vertebrate diversity","authors":"Hugo Sentenac, Dirk S Schmeller, Solène Caubet, Adélaïde Carsin, Rémi Guillet, Jessica Ferriol, Joséphine Leflaive, Adeline Loyau","doi":"10.1093/ismejo/wrae189","DOIUrl":"https://doi.org/10.1093/ismejo/wrae189","url":null,"abstract":"Emerging infectious diseases threaten biodiversity and human health. Many emerging pathogens have aquatic life stages and all immersed substrates have biofilms on their surface, i.e., communities of microorganisms producing a gelatinous matrix. However, the outcome of the interactions between environmental biofilms and pathogens is poorly understood. Here we demonstrate that biofilms reduce the survival of the most impactful pathogen for vertebrate diversity, the invasive chytrid fungus Batrachochytrium dendrobatidis. Effects on its zoospores varied with biofilm composition in controlled settings and biofilm compositional variation also coincided with divergent impacts of chytridiomycosis on amphibian populations in nature. Our results suggest that biofilms form a biotic component of ecosystem resistance to Batrachochytrium dendrobatidis by reducing environmental transmission, and that they could be used to develop nature-based technologies to limit the impacts and spread of this invasive chytrid fungus. Our study warrants further research into the interactions between environmental biofilms and pathogenic and/or invasive micro-organisms.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"25 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2024-09-26","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142325513","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}
Michael Raatz, Amanda de Azevedo-Lopes, Karolina Drabik, Arne Traulsen, Bartlomiej Waclaw
Treatment of urinary tract infections and the prevention of their recurrence is a pressing global health problem. In a urinary infection, pathogenic bacteria not only reside in the bladder lumen but also attach to and invade the bladder tissue. Planktonic, attached, and intracellular bacteria face different selection pressures from physiological processes such as micturition, immune response, and antibiotic treatment. Here, we use a mathematical model of the initial phase of infection to unravel the effects of these different selective pressures on the ecological and evolutionary dynamics of urinary infections. We explicitly model planktonic bacteria in the bladder lumen, bacteria attached to the bladder wall, and bacteria that have invaded the epithelial cells of the bladder. We find that the presence of non-planktonic bacteria substantially increases the risk of infection establishment and affects evolutionary trajectories leading to resistance during antibiotic treatment. We also show that competitive inoculation with a fast-growing non-pathogenic strain can reduce the pathogen load and increase the efficacy of an antibiotic, but only if the antibiotic is used in moderation. Our study shows that including different compartments is essential to create more realistic models of urinary infections, which may help guide new treatment strategies.
{"title":"Pathogen non-planktonic phases within the urinary tract impact early infection and resistance evolution","authors":"Michael Raatz, Amanda de Azevedo-Lopes, Karolina Drabik, Arne Traulsen, Bartlomiej Waclaw","doi":"10.1093/ismejo/wrae191","DOIUrl":"https://doi.org/10.1093/ismejo/wrae191","url":null,"abstract":"Treatment of urinary tract infections and the prevention of their recurrence is a pressing global health problem. In a urinary infection, pathogenic bacteria not only reside in the bladder lumen but also attach to and invade the bladder tissue. Planktonic, attached, and intracellular bacteria face different selection pressures from physiological processes such as micturition, immune response, and antibiotic treatment. Here, we use a mathematical model of the initial phase of infection to unravel the effects of these different selective pressures on the ecological and evolutionary dynamics of urinary infections. We explicitly model planktonic bacteria in the bladder lumen, bacteria attached to the bladder wall, and bacteria that have invaded the epithelial cells of the bladder. We find that the presence of non-planktonic bacteria substantially increases the risk of infection establishment and affects evolutionary trajectories leading to resistance during antibiotic treatment. We also show that competitive inoculation with a fast-growing non-pathogenic strain can reduce the pathogen load and increase the efficacy of an antibiotic, but only if the antibiotic is used in moderation. Our study shows that including different compartments is essential to create more realistic models of urinary infections, which may help guide new treatment strategies.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"42 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2024-09-26","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142325508","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}
C Logan Pierpont, Jacob J Baroch, Matthew J Church, Scott R Miller
Thermophilic microorganisms are expected to have smaller cells and genomes compared with mesophiles, a higher proportion of horizontally acquired genes, and distinct nucleotide and amino acid composition signatures. Here, we took an integrative approach to investigate these apparent correlates of thermophily for Synechococcus A/B cyanobacteria, which include the most heat-tolerant phototrophs on the planet. Phylogenomics confirmed a unique origin of different thermotolerance ecotypes, with low levels of continued gene flow between ecologically divergent but overlapping populations, which has shaped the distribution of phenotypic traits along these geothermal gradients. More thermotolerant strains do have smaller genomes, but genome reduction is associated with a decrease in community richness and metabolic diversity, rather than with cell size. Horizontal gene transfer played only a limited role during Synechococcus evolution, but, the most thermotolerant strains have acquired a Thermus tRNA modification enzyme that may stabilize translation at high temperatures. Although nucleotide base composition was not associated with thermotolerance, we found a general replacement of aspartate with glutamate, as well as a dramatic remodeling of amino acid composition at the highest temperatures that substantially differed from previous predictions. We conclude that Synechococcus A/B genome diversification largely does not conform to the standard view of temperature adaptation. In addition, carbon fixation was more thermolabile than photosynthetic oxygen evolution for the most thermotolerant strains compared with less tolerant lineages. This suggests that increased flow of reducing power generated during the light reactions to an electron sink(s) beyond carbon dioxide has emerged during temperature adaptation of these bacteria.
{"title":"Idiosyncratic genome evolution of the thermophilic cyanobacterium Synechococcus at the limits of phototrophy","authors":"C Logan Pierpont, Jacob J Baroch, Matthew J Church, Scott R Miller","doi":"10.1093/ismejo/wrae184","DOIUrl":"https://doi.org/10.1093/ismejo/wrae184","url":null,"abstract":"Thermophilic microorganisms are expected to have smaller cells and genomes compared with mesophiles, a higher proportion of horizontally acquired genes, and distinct nucleotide and amino acid composition signatures. Here, we took an integrative approach to investigate these apparent correlates of thermophily for Synechococcus A/B cyanobacteria, which include the most heat-tolerant phototrophs on the planet. Phylogenomics confirmed a unique origin of different thermotolerance ecotypes, with low levels of continued gene flow between ecologically divergent but overlapping populations, which has shaped the distribution of phenotypic traits along these geothermal gradients. More thermotolerant strains do have smaller genomes, but genome reduction is associated with a decrease in community richness and metabolic diversity, rather than with cell size. Horizontal gene transfer played only a limited role during Synechococcus evolution, but, the most thermotolerant strains have acquired a Thermus tRNA modification enzyme that may stabilize translation at high temperatures. Although nucleotide base composition was not associated with thermotolerance, we found a general replacement of aspartate with glutamate, as well as a dramatic remodeling of amino acid composition at the highest temperatures that substantially differed from previous predictions. We conclude that Synechococcus A/B genome diversification largely does not conform to the standard view of temperature adaptation. In addition, carbon fixation was more thermolabile than photosynthetic oxygen evolution for the most thermotolerant strains compared with less tolerant lineages. This suggests that increased flow of reducing power generated during the light reactions to an electron sink(s) beyond carbon dioxide has emerged during temperature adaptation of these bacteria.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"8 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2024-09-25","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142317576","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}
Telonemia are one of the oldest identified marine protists that for most part of their history have been recognized as a distinct incertae sedis lineage. Today, their evolutionary proximity to the SAR supergroup (Stramenopiles, Alveolates, and Rhizaria) is firmly established. However, their ecological distribution and importance as a natural predatory flagellate, especially in freshwater food webs, still remains unclear. To unravel the distribution and diversity of the phylum Telonemia in freshwater habitats, we examined over a thousand freshwater metagenomes from all over the world. In addition, to directly quantify absolute abundances, we analysed 407 samples from 97 lakes and reservoirs using Catalyzed Reporter Deposition-Fluorescence in situ Hybridization (CARD-FISH). We recovered Telonemia 18S rRNA gene sequences from hundreds of metagenomic samples from a wide variety of habitats, indicating a global distribution of this phylum. However, even after this extensive sampling, our phylogenetic analysis did not reveal any new major clades, suggesting current molecular surveys are near to capturing the full diversity within this group. We observed excellent concordance between CARD-FISH analyses and estimates of abundances from metagenomes. Both approaches suggest that Telonemia are largely absent from shallow lakes and prefer to inhabit the colder hypolimnion of lakes and reservoirs in the Northern Hemisphere, where they frequently bloom, reaching 10-20% of the total heterotrophic flagellate population, making them important predatory flagellates in the freshwater food web.
{"title":"Global freshwater distribution of Telonemia protists.","authors":"Roudaina Boukheloua,Indranil Mukherjee,Hongjae Park,Karel Šimek,Vojtěch Kasalický,Maxon Ngochera,Hans-Peter Grossart,Antonio Picazo-Mozo,Antonio Camacho,Pedro J Cabello-Yeves,Francisco Rodriguez-Valera,Cristiana Callieri,Adrian-Stefan Andrei,Jakob Pernthaler,Thomas Posch,Albin Alfreider,Ruben Sommaruga,Martin W Hahn,Bettina Sonntag,Purificacion Lopez-Garcia,David Moreira,Ludwig Jardillier,Cécile Lepère,Corinne Biderre-Petit,Anna Bednarska,Mirosław Ślusarczyk,Viktor R Tóth,Horia L Banciu,Konstantinos Kormas,Sandi Orlic,Danijela Šantić,Gerard Muyzer,Daniel P R Herlemann,Helen Tammert,Stefan Bertilsson,Silke Langenheder,Thomas Zechmeister,Nico Salmaso,Nicola Storelli,Camilla Capelli,Fabio Lepori,Vojtěch Lanta,Helena Henriques Vieira,Fran Kostanjšek,Kateřina Kabeláčová,Maria-Cecilia Chiriac,Markus Haber,Tanja Shabarova,Clafy Fernandes,Pavel Rychtecký,Petr Znachor,Tiberiu Szőke-Nagy,Paul Layoun,Hon Lun Wong,Vinicius Silva Kavagutti,Paul-Adrian Bulzu,Michaela M Salcher,Kasia Piwosz,Rohit Ghai","doi":"10.1093/ismejo/wrae177","DOIUrl":"https://doi.org/10.1093/ismejo/wrae177","url":null,"abstract":"Telonemia are one of the oldest identified marine protists that for most part of their history have been recognized as a distinct incertae sedis lineage. Today, their evolutionary proximity to the SAR supergroup (Stramenopiles, Alveolates, and Rhizaria) is firmly established. However, their ecological distribution and importance as a natural predatory flagellate, especially in freshwater food webs, still remains unclear. To unravel the distribution and diversity of the phylum Telonemia in freshwater habitats, we examined over a thousand freshwater metagenomes from all over the world. In addition, to directly quantify absolute abundances, we analysed 407 samples from 97 lakes and reservoirs using Catalyzed Reporter Deposition-Fluorescence in situ Hybridization (CARD-FISH). We recovered Telonemia 18S rRNA gene sequences from hundreds of metagenomic samples from a wide variety of habitats, indicating a global distribution of this phylum. However, even after this extensive sampling, our phylogenetic analysis did not reveal any new major clades, suggesting current molecular surveys are near to capturing the full diversity within this group. We observed excellent concordance between CARD-FISH analyses and estimates of abundances from metagenomes. Both approaches suggest that Telonemia are largely absent from shallow lakes and prefer to inhabit the colder hypolimnion of lakes and reservoirs in the Northern Hemisphere, where they frequently bloom, reaching 10-20% of the total heterotrophic flagellate population, making them important predatory flagellates in the freshwater food web.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"48 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2024-09-20","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142275207","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 are undergoing unprecedented dispersion and amalgamation across diverse ecosystems, thereby exerting profound and pervasive influences on microbial assemblages and ecosystem dynamics. This review delves into the phenomenon of community coalescence, offering an ecological overview that outlines its four-step process and elucidates the intrinsic interconnections in the context of community assembly. We examine pivotal mechanisms driving community coalescence, with a particular emphasis on elucidating the fates of both source and resident microbial communities and the consequential impacts on the ecosystem. Finally, we proffer recommendations to guide researchers in this rapidly evolving domain, facilitating deeper insights into the ecological ramifications of microbial community coalescence.
{"title":"Drivers and consequences of microbial community coalescence","authors":"Xipeng Liu, Joana Falcão Salles","doi":"10.1093/ismejo/wrae179","DOIUrl":"https://doi.org/10.1093/ismejo/wrae179","url":null,"abstract":"Microbial communities are undergoing unprecedented dispersion and amalgamation across diverse ecosystems, thereby exerting profound and pervasive influences on microbial assemblages and ecosystem dynamics. This review delves into the phenomenon of community coalescence, offering an ecological overview that outlines its four-step process and elucidates the intrinsic interconnections in the context of community assembly. We examine pivotal mechanisms driving community coalescence, with a particular emphasis on elucidating the fates of both source and resident microbial communities and the consequential impacts on the ecosystem. Finally, we proffer recommendations to guide researchers in this rapidly evolving domain, facilitating deeper insights into the ecological ramifications of microbial community coalescence.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"54 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2024-09-17","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142236694","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}
Dagmar Čížková, Pavel Payne, Anna Bryjová, Ľudovít Ďureje, Jaroslav Piálek, Jakub Kreisinger
Bacteriophages are abundant components of vertebrate gut microbial communities, impacting bacteriome dynamics, evolution, and directly interacting with the superhost. However, knowledge about gut phageomes and their interaction with bacteriomes in vertebrates under natural conditions is limited to humans and non-human primates. Widely used specific pathogen-free (SPF) mouse models of host-microbiota interactions have altered gut bacteriomes compared to wild mice, and data on phageomes from wild or other non-SPF mice are lacking. We demonstrate divergent gut phageomes and bacteriomes in wild and captive non-SPF mice, with wild mice phageomes exhibiting higher alpha-diversity and interindividual variability. In both groups, phageome and bacteriome structuring mirrored each other, correlating at the individual level. Re-analysis of previous data from phageomes of SPF mice revealed their enrichment in Suoliviridae crAss-like phages compared to our non-SPF mice. Disrupted bacteriomes in mouse models can be treated by transplanting healthy phageomes, but the effects of phageome transplants on healthy adult gut microbiota are still unknown. We show that experimental transplantation of phageomes from wild to captive mice did not cause major shifts in recipient phageomes. However, the convergence of recipient-to-donor phageomes confirmed that wild phages can integrate into recipient communities. The differences in the subset of integrated phages between the two recipient mouse strains illustrate the context-dependent effects of phage transplantation. The transplantation did not impact recipient gut bacteriomes. This resilience of healthy adult gut microbiomes to the intervention has implications for phage allotransplantation safety.
{"title":"Convergence of gut phage communities but not bacterial communities following wild mouse bacteriophage transplantation into captive house mice","authors":"Dagmar Čížková, Pavel Payne, Anna Bryjová, Ľudovít Ďureje, Jaroslav Piálek, Jakub Kreisinger","doi":"10.1093/ismejo/wrae178","DOIUrl":"https://doi.org/10.1093/ismejo/wrae178","url":null,"abstract":"Bacteriophages are abundant components of vertebrate gut microbial communities, impacting bacteriome dynamics, evolution, and directly interacting with the superhost. However, knowledge about gut phageomes and their interaction with bacteriomes in vertebrates under natural conditions is limited to humans and non-human primates. Widely used specific pathogen-free (SPF) mouse models of host-microbiota interactions have altered gut bacteriomes compared to wild mice, and data on phageomes from wild or other non-SPF mice are lacking. We demonstrate divergent gut phageomes and bacteriomes in wild and captive non-SPF mice, with wild mice phageomes exhibiting higher alpha-diversity and interindividual variability. In both groups, phageome and bacteriome structuring mirrored each other, correlating at the individual level. Re-analysis of previous data from phageomes of SPF mice revealed their enrichment in Suoliviridae crAss-like phages compared to our non-SPF mice. Disrupted bacteriomes in mouse models can be treated by transplanting healthy phageomes, but the effects of phageome transplants on healthy adult gut microbiota are still unknown. We show that experimental transplantation of phageomes from wild to captive mice did not cause major shifts in recipient phageomes. However, the convergence of recipient-to-donor phageomes confirmed that wild phages can integrate into recipient communities. The differences in the subset of integrated phages between the two recipient mouse strains illustrate the context-dependent effects of phage transplantation. The transplantation did not impact recipient gut bacteriomes. This resilience of healthy adult gut microbiomes to the intervention has implications for phage allotransplantation safety.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"115 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2024-09-14","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142233356","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}
Katja Laufer-Meiser, Malik Alawi, Stefanie Böhnke, Claus-Henning Solterbeck, Jana Schloesser, Axel Schippers, Philipp Dirksen, Thomas Brüser, Susann Henkel, Janina Fuss, Mirjam Perner
Chemolithoautotrophic Hydrogenovibrio are ubiquitous and abundant at hydrothermal vents. They can oxidize sulfur, hydrogen or iron, but none are known to use all three energy sources. This ability though would be advantageous in vents hallmarked by highly dynamic environmental conditions. We isolated three Hydrogenovibrio strains from vents along the Indian Ridge, which grow on all three electron donors. We present transcriptomic data from strains grown on iron, hydrogen or thiosulfate with respective oxidation and autotrophic CO2 fixation rates, RubisCO activity, SEM, and EDX. Maximum estimates of one strain’s oxidation potential were 10, 24, and 952 mmol for iron, hydrogen and thiosulfate oxidation and 0.3, 1, and 84 mmol CO2 fixation, respectively, per vent per hour indicating their relevance for element cycling in-situ. Several genes were up- or downregulated depending on the inorganic electron donor provided. Although no known genes of iron-oxidation were detected, upregulated transcripts suggested iron-acquisition and so far unknown iron-oxidation-pathways.
{"title":"Oxidation of sulfur, hydrogen, and iron by metabolically versatile Hydrogenovibrio from deep sea hydrothermal vents","authors":"Katja Laufer-Meiser, Malik Alawi, Stefanie Böhnke, Claus-Henning Solterbeck, Jana Schloesser, Axel Schippers, Philipp Dirksen, Thomas Brüser, Susann Henkel, Janina Fuss, Mirjam Perner","doi":"10.1093/ismejo/wrae173","DOIUrl":"https://doi.org/10.1093/ismejo/wrae173","url":null,"abstract":"Chemolithoautotrophic Hydrogenovibrio are ubiquitous and abundant at hydrothermal vents. They can oxidize sulfur, hydrogen or iron, but none are known to use all three energy sources. This ability though would be advantageous in vents hallmarked by highly dynamic environmental conditions. We isolated three Hydrogenovibrio strains from vents along the Indian Ridge, which grow on all three electron donors. We present transcriptomic data from strains grown on iron, hydrogen or thiosulfate with respective oxidation and autotrophic CO2 fixation rates, RubisCO activity, SEM, and EDX. Maximum estimates of one strain’s oxidation potential were 10, 24, and 952 mmol for iron, hydrogen and thiosulfate oxidation and 0.3, 1, and 84 mmol CO2 fixation, respectively, per vent per hour indicating their relevance for element cycling in-situ. Several genes were up- or downregulated depending on the inorganic electron donor provided. Although no known genes of iron-oxidation were detected, upregulated transcripts suggested iron-acquisition and so far unknown iron-oxidation-pathways.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"4 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2024-09-12","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142233344","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}
Lisa-Marie Delpech,Alexander T Tveit,Andrew J Hodson,Kevin P Hand,Dimitri Kalenitchenko
Below their ice shells, icy moons may offer a source of chemical energy that could support microbial life in the absence of light. In the Arctic, past and present glacial retreat leads to isostatic uplift of sediments through which cold and methane-saturated groundwater travels. This fluid reaches the surface and freezes as hill-shaped icings during winter, producing dark ice-water interfaces above water ponds containing chemical energy sources. In one such system characterized by elevated methane concentrations - the Lagoon Pingo in Adventdalen, Svalbard (~10 mg/L CH4, <0.3 mg/L O2, -0.25°C, pH 7.9), we studied amplicons of the bacterial and archaeal (microbial) 16S rRNA gene and transcripts in the water pond and overlaying ice. We show that active chemolithoautotrophic sulfur-oxidizing microorganisms (Sulfurimonas, Thiomicrorhabdus) dominated a niche at the bottom of the ice in contact with the anoxic water reservoir. There, the growing ice offers surfaces interfacing with water, and hosts favorable physico-chemical conditions for sulfide oxidation. Detection of anaerobic methanotrophs further suggests that the ice led to a steady-state dark and cold methane sink under the ice throughout winter, in two steps: first methane is oxidized to carbon dioxide and sulfates concomitantly reduced to sulfides by the activity of ANME-1a and SEEP-SRB1 consortia, in a second time energy from sulfides is used by sulfur- oxidizing microorganisms to fix carbon dioxide into organic carbon. Our results underline ice- covered and dark ecosystems as a hitherto overlooked oasis of microbial life and emphasize the need to study microbial communities in icy habitats.
{"title":"Chemolithoautotrophic bacteria flourish at dark water-ice interfaces of an emerged Arctic cold seep.","authors":"Lisa-Marie Delpech,Alexander T Tveit,Andrew J Hodson,Kevin P Hand,Dimitri Kalenitchenko","doi":"10.1093/ismejo/wrae170","DOIUrl":"https://doi.org/10.1093/ismejo/wrae170","url":null,"abstract":"Below their ice shells, icy moons may offer a source of chemical energy that could support microbial life in the absence of light. In the Arctic, past and present glacial retreat leads to isostatic uplift of sediments through which cold and methane-saturated groundwater travels. This fluid reaches the surface and freezes as hill-shaped icings during winter, producing dark ice-water interfaces above water ponds containing chemical energy sources. In one such system characterized by elevated methane concentrations - the Lagoon Pingo in Adventdalen, Svalbard (~10 mg/L CH4, <0.3 mg/L O2, -0.25°C, pH 7.9), we studied amplicons of the bacterial and archaeal (microbial) 16S rRNA gene and transcripts in the water pond and overlaying ice. We show that active chemolithoautotrophic sulfur-oxidizing microorganisms (Sulfurimonas, Thiomicrorhabdus) dominated a niche at the bottom of the ice in contact with the anoxic water reservoir. There, the growing ice offers surfaces interfacing with water, and hosts favorable physico-chemical conditions for sulfide oxidation. Detection of anaerobic methanotrophs further suggests that the ice led to a steady-state dark and cold methane sink under the ice throughout winter, in two steps: first methane is oxidized to carbon dioxide and sulfates concomitantly reduced to sulfides by the activity of ANME-1a and SEEP-SRB1 consortia, in a second time energy from sulfides is used by sulfur- oxidizing microorganisms to fix carbon dioxide into organic carbon. Our results underline ice- covered and dark ecosystems as a hitherto overlooked oasis of microbial life and emphasize the need to study microbial communities in icy habitats.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"6 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2024-09-12","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142233347","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}
Michael P Thorgersen, Jennifer L Goff, Valentine V Trotter, Farris L Poole, Adam P Arkin, Adam M Deutschbauer, Michael W W Adams
Many factors contribute to the ability of a microbial species to persist when encountering complexly contaminated environments including time of exposure, the nature and concentration of contaminants, availability of nutritional resources, and possession of a combination of appropriate molecular mechanisms needed for survival. Herein we sought to identify genes that are most important for survival of Gram-negative Enterobacteriaceae in contaminated groundwater environments containing high concentrations of nitrate and metals using the metal-tolerant Oak Ridge Reservation (ORR) isolate, Pantoea sp. MT58 (MT58). Survival fitness experiments in which a randomly barcoded transposon insertion (RB-TnSeq) library of MT58 was exposed directly to contaminated ORR groundwater samples from across a nitrate and mixed metal contamination plume were used to identify genes important for survival with increasing exposure times and concentrations of contaminants, and availability of a carbon source. Genes involved in controlling and using carbon, encoding transcriptional regulators, and related to Gram-negative outer membrane processes were among those found to be important for survival in contaminated ORR groundwater. A comparative genomics analysis of 75 Pantoea genus strains allowed us to further separate the survival determinants into core and non-core genes in the Pantoea pangenome, revealing insights into the survival of subsurface microorganisms during contaminant plume intrusion.
{"title":"Fitness factors impacting survival of a subsurface bacterium in contaminated groundwater","authors":"Michael P Thorgersen, Jennifer L Goff, Valentine V Trotter, Farris L Poole, Adam P Arkin, Adam M Deutschbauer, Michael W W Adams","doi":"10.1093/ismejo/wrae176","DOIUrl":"https://doi.org/10.1093/ismejo/wrae176","url":null,"abstract":"Many factors contribute to the ability of a microbial species to persist when encountering complexly contaminated environments including time of exposure, the nature and concentration of contaminants, availability of nutritional resources, and possession of a combination of appropriate molecular mechanisms needed for survival. Herein we sought to identify genes that are most important for survival of Gram-negative Enterobacteriaceae in contaminated groundwater environments containing high concentrations of nitrate and metals using the metal-tolerant Oak Ridge Reservation (ORR) isolate, Pantoea sp. MT58 (MT58). Survival fitness experiments in which a randomly barcoded transposon insertion (RB-TnSeq) library of MT58 was exposed directly to contaminated ORR groundwater samples from across a nitrate and mixed metal contamination plume were used to identify genes important for survival with increasing exposure times and concentrations of contaminants, and availability of a carbon source. Genes involved in controlling and using carbon, encoding transcriptional regulators, and related to Gram-negative outer membrane processes were among those found to be important for survival in contaminated ORR groundwater. A comparative genomics analysis of 75 Pantoea genus strains allowed us to further separate the survival determinants into core and non-core genes in the Pantoea pangenome, revealing insights into the survival of subsurface microorganisms during contaminant plume intrusion.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"28 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2024-09-12","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142174737","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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