Photosymbiosis, a mode of mixotrophy by algal endosymbiosis, provides key advantage to pelagic life in oligotrophic oceans. Despite its ecological importance, mechanisms underlying its emergence and association with the evolutionary success of photosymbiotic lineages remain unclear. We used planktonic foraminifera, a group of pelagic test-forming protists with an excellent fossil record, to reveal the history of symbiont acquisition among their three main extant clades. We used single-cell 18S rRNA gene amplicon sequencing to reveal symbiont identity and mapped the symbiosis on a phylogeny time-calibrated by fossil data. We show that the highly specific symbiotic interaction with dinoflagellates emerged in the wake of a major extinction of symbiont-bearing taxa at the end of the Eocene. In contrast, less specific and low-light adapted symbioses with pelagophytes emerged 20 million years later, in multiple independent lineages in the Late Neogene, at a time when the vertical structure of pelagic ecosystems was transformed by global cooling. We infer that in foraminifera, photosymbiosis can evolve easily and that its establishment leads to diversification and ecological dominance to such extent, that the proliferation of new symbioses is prevented by the incumbent lineages.
{"title":"Two waves of photosymbiosis acquisition in extant planktonic foraminifera explained by ecological incumbency","authors":"Haruka Takagi, Yasuhide Nakamura, Christiane Schmidt, Michal Kucera, Hiroaki Saito, Kazuyoshi Moriya","doi":"10.1093/ismejo/wrae244","DOIUrl":"https://doi.org/10.1093/ismejo/wrae244","url":null,"abstract":"Photosymbiosis, a mode of mixotrophy by algal endosymbiosis, provides key advantage to pelagic life in oligotrophic oceans. Despite its ecological importance, mechanisms underlying its emergence and association with the evolutionary success of photosymbiotic lineages remain unclear. We used planktonic foraminifera, a group of pelagic test-forming protists with an excellent fossil record, to reveal the history of symbiont acquisition among their three main extant clades. We used single-cell 18S rRNA gene amplicon sequencing to reveal symbiont identity and mapped the symbiosis on a phylogeny time-calibrated by fossil data. We show that the highly specific symbiotic interaction with dinoflagellates emerged in the wake of a major extinction of symbiont-bearing taxa at the end of the Eocene. In contrast, less specific and low-light adapted symbioses with pelagophytes emerged 20 million years later, in multiple independent lineages in the Late Neogene, at a time when the vertical structure of pelagic ecosystems was transformed by global cooling. We infer that in foraminifera, photosymbiosis can evolve easily and that its establishment leads to diversification and ecological dominance to such extent, that the proliferation of new symbioses is prevented by the incumbent lineages.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"5 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2024-12-11","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142805405","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}
David Kneis, Faina Tskhay, Magali de la Cruz Barron, Thomas U Berendonk
It is consensus that clinically relevant antibiotic resistance genes have their origin in environmental bacteria, including the large pool of primarily benign species. Yet, for the vast majority of acquired antibiotic resistance genes, the original environmental host(s) have not been identified to date. Closing this knowledge gap could improve our understanding of how antimicrobial resistance proliferates in the bacterial domain and shed light on the crucial step of initial resistance gene mobilization in particular. Here, we combine information from publicly available long- and short-read environmental metagenomes as well as whole-genome sequences to identify the original environmental hosts of dfrB, a family of genes conferring resistance to trimethoprim. Although this gene family stands in the shadow of the more widespread, structurally different dfrA, it has recently gained attention through the discovery of several new members. Based on the genetic context of dfrB observed in long-read metagenomes, we predicted bacteria of the order Burkholderiales to function as original environmental hosts of the predominant gene variants in both soil and freshwater. The predictions were independently confirmed by whole-genome datasets and statistical correlations between dfrB abundance and taxonomic composition of environmental bacterial communities. Our study suggests that Burkholderiales in general and the family Comamonadaceae in particular represent environmental origins of dfrB genes, some of which now contribute to the acquired resistome of facultative pathogens. We propose that our workflow centered around long-read environmental metagenomes allows for the identification of the original hosts of further clinically relevant antibiotic resistance genes.
{"title":"Bacteria of the order Burkholderiales are original environmental hosts of type II trimethoprim resistance genes (dfrB)","authors":"David Kneis, Faina Tskhay, Magali de la Cruz Barron, Thomas U Berendonk","doi":"10.1093/ismejo/wrae243","DOIUrl":"https://doi.org/10.1093/ismejo/wrae243","url":null,"abstract":"It is consensus that clinically relevant antibiotic resistance genes have their origin in environmental bacteria, including the large pool of primarily benign species. Yet, for the vast majority of acquired antibiotic resistance genes, the original environmental host(s) have not been identified to date. Closing this knowledge gap could improve our understanding of how antimicrobial resistance proliferates in the bacterial domain and shed light on the crucial step of initial resistance gene mobilization in particular. Here, we combine information from publicly available long- and short-read environmental metagenomes as well as whole-genome sequences to identify the original environmental hosts of dfrB, a family of genes conferring resistance to trimethoprim. Although this gene family stands in the shadow of the more widespread, structurally different dfrA, it has recently gained attention through the discovery of several new members. Based on the genetic context of dfrB observed in long-read metagenomes, we predicted bacteria of the order Burkholderiales to function as original environmental hosts of the predominant gene variants in both soil and freshwater. The predictions were independently confirmed by whole-genome datasets and statistical correlations between dfrB abundance and taxonomic composition of environmental bacterial communities. Our study suggests that Burkholderiales in general and the family Comamonadaceae in particular represent environmental origins of dfrB genes, some of which now contribute to the acquired resistome of facultative pathogens. We propose that our workflow centered around long-read environmental metagenomes allows for the identification of the original hosts of further clinically relevant antibiotic resistance genes.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"38 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2024-12-11","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142805407","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}
Keith Dufault-Thompson, Sophia Levy, Brantley Hall, Xiaofang Jiang
Animal gastrointestinal tracts contain diverse metabolites, including various host-derived compounds that gut-associated microbes interact with. Here, we explore the diversity and evolution of bilirubin reductase, a bacterial enzyme that metabolizes the host-derived tetrapyrrole bilirubin, performing a key role in the animal heme degradation pathway. Through an analysis of the bilirubin reductase phylogeny and predicted structures, we found that the enzyme family can be divided into three distinct clades with different structural features. Using these clade definitions, we analyzed metagenomic sequencing data from multiple animal species, finding that bilirubin reductase is significantly enriched in the large intestines of animals and that the clades exhibit differences in distribution among animals. Combined with phylogenetic signal analysis, we find that the bilirubin reductase clades exhibit significant associations with specific animals and animal physiological traits like gastrointestinal anatomy and diet. These patterns demonstrate that bilirubin reductase is specifically adapted to the anoxic lower gut environment of animals and that its evolutionary history is complex, involving adaptation to a diverse collection of animals harboring bilirubin-reducing microbes. The findings suggest that bilirubin reductase evolution has been shaped by the host environment, providing a new perspective on heme metabolism in animals and highlighting the importance of the microbiome in animal physiology and evolution.
{"title":"Bilirubin Reductase Shows Host-Specific Associations in Animal Large Intestines","authors":"Keith Dufault-Thompson, Sophia Levy, Brantley Hall, Xiaofang Jiang","doi":"10.1093/ismejo/wrae242","DOIUrl":"https://doi.org/10.1093/ismejo/wrae242","url":null,"abstract":"Animal gastrointestinal tracts contain diverse metabolites, including various host-derived compounds that gut-associated microbes interact with. Here, we explore the diversity and evolution of bilirubin reductase, a bacterial enzyme that metabolizes the host-derived tetrapyrrole bilirubin, performing a key role in the animal heme degradation pathway. Through an analysis of the bilirubin reductase phylogeny and predicted structures, we found that the enzyme family can be divided into three distinct clades with different structural features. Using these clade definitions, we analyzed metagenomic sequencing data from multiple animal species, finding that bilirubin reductase is significantly enriched in the large intestines of animals and that the clades exhibit differences in distribution among animals. Combined with phylogenetic signal analysis, we find that the bilirubin reductase clades exhibit significant associations with specific animals and animal physiological traits like gastrointestinal anatomy and diet. These patterns demonstrate that bilirubin reductase is specifically adapted to the anoxic lower gut environment of animals and that its evolutionary history is complex, involving adaptation to a diverse collection of animals harboring bilirubin-reducing microbes. The findings suggest that bilirubin reductase evolution has been shaped by the host environment, providing a new perspective on heme metabolism in animals and highlighting the importance of the microbiome in animal physiology and evolution.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"9 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2024-12-11","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142805406","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}
Giant viruses can control their eukaryotic host populations, shaping the ecology and evolution of aquatic microbial communities. Understanding the impact of the viruses’ own parasites, the virophages, on the control of microbial communities remains a challenge. Most virophages have two modes of infection. They can exist as free particles coinfecting host cells together with the virus, where they replicate while inhibiting viral replication. Virophages can also integrate into the host genome, replicate through host cell division and remain dormant until the host is infected with a virus, leading to virophage reactivation and replication without inhibiting viral replication. Both infection modes (reactivation vs. coinfection) occur within host-virus-virophage communities, and their relative contributions are expected to be dynamic and context dependent. The consequences of this dynamic regime for ecological and evolutionary dynamics remain unexplored. Here, we test whether and how the relative contribution of virophage infection modes influences the ecological dynamics of an experimental host-virus-virophage system and the evolutionary responses of the virophage. We indirectly manipulated the level of virophage (Mavirus) integration into the host (Cafeteria burkhardae) in the presence of the giant Cafeteria roenbergensis virus. Communities with higher virophage integration were characterised by lower population densities and reduced fluctuations in host and virus populations, whereas virophage fluctuations were increased. The virophage evolved toward lower inhibition and higher replication, but the evolution of these traits was weaker with higher virophage integration. Our study shows that differences in the virophage infection modes contributes to the complex interplay between virophages, viruses and hosts.
{"title":"Virophage infection mode determines ecological and evolutionary changes in a host-virus-virophage system","authors":"Ana del Arco, Lutz Becks","doi":"10.1093/ismejo/wrae237","DOIUrl":"https://doi.org/10.1093/ismejo/wrae237","url":null,"abstract":"Giant viruses can control their eukaryotic host populations, shaping the ecology and evolution of aquatic microbial communities. Understanding the impact of the viruses’ own parasites, the virophages, on the control of microbial communities remains a challenge. Most virophages have two modes of infection. They can exist as free particles coinfecting host cells together with the virus, where they replicate while inhibiting viral replication. Virophages can also integrate into the host genome, replicate through host cell division and remain dormant until the host is infected with a virus, leading to virophage reactivation and replication without inhibiting viral replication. Both infection modes (reactivation vs. coinfection) occur within host-virus-virophage communities, and their relative contributions are expected to be dynamic and context dependent. The consequences of this dynamic regime for ecological and evolutionary dynamics remain unexplored. Here, we test whether and how the relative contribution of virophage infection modes influences the ecological dynamics of an experimental host-virus-virophage system and the evolutionary responses of the virophage. We indirectly manipulated the level of virophage (Mavirus) integration into the host (Cafeteria burkhardae) in the presence of the giant Cafeteria roenbergensis virus. Communities with higher virophage integration were characterised by lower population densities and reduced fluctuations in host and virus populations, whereas virophage fluctuations were increased. The virophage evolved toward lower inhibition and higher replication, but the evolution of these traits was weaker with higher virophage integration. Our study shows that differences in the virophage infection modes contributes to the complex interplay between virophages, viruses and hosts.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"119 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2024-12-10","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142805409","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 importance of rare earth elements is increasingly recognized due to the increased demand for their mining and separation. This demand is driving research on the biology of rare earth elements. Biomolecules associated with rare earth elements include rare earth element-dependent enzymes (methanol dehydrogenase XoxF, ethanol dehydrogenase ExaF/PedH), rare earth element-binding proteins, and the relevant metallophores. Traditional (chemical) separation methods for rare earth elements harvesting and separation are typically inefficient, while causing environmental problems, whereas bioharvesting, potentially, offers more efficient, more green platforms. Here, we review the current state of research on the biological functions of rare earth element-dependent biomolecules, and the characteristics of the relevant proteins, including the specific amino acids involved in rare earth metal binding. We also provide an outlook at strategies for further understanding of biological processes and the potential applications of rare earth element-dependent enzymes and other biomolecules.
{"title":"Emerging role of rare earth elements in biomolecular functions","authors":"Wenyu Yang, Kaijuan Wu, Hao Chen, Jing Huang, Zheng Yu","doi":"10.1093/ismejo/wrae241","DOIUrl":"https://doi.org/10.1093/ismejo/wrae241","url":null,"abstract":"The importance of rare earth elements is increasingly recognized due to the increased demand for their mining and separation. This demand is driving research on the biology of rare earth elements. Biomolecules associated with rare earth elements include rare earth element-dependent enzymes (methanol dehydrogenase XoxF, ethanol dehydrogenase ExaF/PedH), rare earth element-binding proteins, and the relevant metallophores. Traditional (chemical) separation methods for rare earth elements harvesting and separation are typically inefficient, while causing environmental problems, whereas bioharvesting, potentially, offers more efficient, more green platforms. Here, we review the current state of research on the biological functions of rare earth element-dependent biomolecules, and the characteristics of the relevant proteins, including the specific amino acids involved in rare earth metal binding. We also provide an outlook at strategies for further understanding of biological processes and the potential applications of rare earth element-dependent enzymes and other biomolecules.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"24 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2024-12-10","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142805408","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}
Natascha S Varona, Poppy J Hesketh-Best, Felipe H Coutinho, Alexandra K Stiffler, Bailey A Wallace, Sofia L Garcia, Yun Scholten, Andreas F Haas, Mark Little, Mark Vermeij, Antoni Luque, Cynthia Silveira
Viral infections are major modulators of marine microbial community assembly and biogeochemical cycling. In coral reefs, viral lysis controls bacterial overgrowth that is detrimental to coral health. However, methodological limitations have prevented the identification of viral hosts and quantification of their interaction frequencies. Here, we reconstructed an abundance-resolved virus-bacteria interaction network in the oligotrophic coral reef waters of Curaçao by integrating direct microscopy counts with virus-host links obtained from proximity-ligation, prophage integration, and CRISPR spacers. This network of 3,013 individual links (97 unique species-level interactions) revealed that the abundance of free viral particles was weakly related to host abundance and viral production, as indicated by the cell-associated virus-to-host ratio. The viruses with the highest free and cell-associated virus-to-host ratio, interpreted here as highly productive viruses, formed links with intermediate-to-low abundance hosts belonging to Gammaproteobacteria, Bacteroidia, and Planctomycetia. In contrast, low-production viruses interacted with abundant members of Alphaproteobacteria and Gammaproteobacteria enriched in prophages. These findings highlight the decoupling between viral abundance and production and identify potentially active viruses. We propose that differential decay rates and burst sizes may explain the decoupling between free viral abundance and production and that lysogenic infections play an important role in the ecology of high-abundance hosts.
{"title":"Host-specific viral predation network on coral reefs","authors":"Natascha S Varona, Poppy J Hesketh-Best, Felipe H Coutinho, Alexandra K Stiffler, Bailey A Wallace, Sofia L Garcia, Yun Scholten, Andreas F Haas, Mark Little, Mark Vermeij, Antoni Luque, Cynthia Silveira","doi":"10.1093/ismejo/wrae240","DOIUrl":"https://doi.org/10.1093/ismejo/wrae240","url":null,"abstract":"Viral infections are major modulators of marine microbial community assembly and biogeochemical cycling. In coral reefs, viral lysis controls bacterial overgrowth that is detrimental to coral health. However, methodological limitations have prevented the identification of viral hosts and quantification of their interaction frequencies. Here, we reconstructed an abundance-resolved virus-bacteria interaction network in the oligotrophic coral reef waters of Curaçao by integrating direct microscopy counts with virus-host links obtained from proximity-ligation, prophage integration, and CRISPR spacers. This network of 3,013 individual links (97 unique species-level interactions) revealed that the abundance of free viral particles was weakly related to host abundance and viral production, as indicated by the cell-associated virus-to-host ratio. The viruses with the highest free and cell-associated virus-to-host ratio, interpreted here as highly productive viruses, formed links with intermediate-to-low abundance hosts belonging to Gammaproteobacteria, Bacteroidia, and Planctomycetia. In contrast, low-production viruses interacted with abundant members of Alphaproteobacteria and Gammaproteobacteria enriched in prophages. These findings highlight the decoupling between viral abundance and production and identify potentially active viruses. We propose that differential decay rates and burst sizes may explain the decoupling between free viral abundance and production and that lysogenic infections play an important role in the ecology of high-abundance hosts.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"200 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2024-12-10","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142805441","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}
Caroline Juéry, Adria Auladell, Zoltan Füssy, Fabien Chevalier, Daniel P Yee, Eric Pelletier, Erwan Corre, Andrew E Allen, Daniel J Richter, Johan Decelle
Metabolic exchange is one of the foundations of symbiotic associations between organisms and is a driving force in evolution. In the ocean, photosymbiosis between heterotrophic hosts and microalgae is powered by photosynthesis and relies on the transfer of organic carbon to the host (e.g. sugars). Yet, the identity of transferred carbohydrates as well as the molecular mechanisms that drive this exchange remain largely unknown, especially in unicellular photosymbioses that are widespread in the open ocean. Combining genomics, single-holobiont transcriptomics, and environmental metatranscriptomics, we revealed the transportome of the marine microalga Phaeocystis in symbiosis within acantharia, with a focus on sugar transporters. At the genomic level, the sugar transportome of Phaeocystis is comparable to non-symbiotic haptophytes. By contrast, we found significant remodeling of the expression of the transportome in symbiotic microalgae compared to the free-living stage. More particularly, 36% of sugar transporter genes were differentially expressed. Several of them, such as GLUTs, TPTs, and aquaporins, with glucose, triose-phosphate sugars, and glycerol as potential substrates, were upregulated at the holobiont and community level. We also showed that algal sugar transporter genes exhibit distinct temporal expression patterns during the day. This reprogrammed transportome indicates that symbiosis has a major impact on sugar fluxes within and outside the algal cell, and highlights the complexity and the dynamics of metabolic exchanges between partners. This study improves our understanding of the molecular players of the metabolic connectivity underlying the ecological success of planktonic photosymbiosis and paves the way for more studies on transporters across photosymbiotic models.
{"title":"Transportome remodeling of a symbiotic microalga inside a planktonic host","authors":"Caroline Juéry, Adria Auladell, Zoltan Füssy, Fabien Chevalier, Daniel P Yee, Eric Pelletier, Erwan Corre, Andrew E Allen, Daniel J Richter, Johan Decelle","doi":"10.1093/ismejo/wrae239","DOIUrl":"https://doi.org/10.1093/ismejo/wrae239","url":null,"abstract":"Metabolic exchange is one of the foundations of symbiotic associations between organisms and is a driving force in evolution. In the ocean, photosymbiosis between heterotrophic hosts and microalgae is powered by photosynthesis and relies on the transfer of organic carbon to the host (e.g. sugars). Yet, the identity of transferred carbohydrates as well as the molecular mechanisms that drive this exchange remain largely unknown, especially in unicellular photosymbioses that are widespread in the open ocean. Combining genomics, single-holobiont transcriptomics, and environmental metatranscriptomics, we revealed the transportome of the marine microalga Phaeocystis in symbiosis within acantharia, with a focus on sugar transporters. At the genomic level, the sugar transportome of Phaeocystis is comparable to non-symbiotic haptophytes. By contrast, we found significant remodeling of the expression of the transportome in symbiotic microalgae compared to the free-living stage. More particularly, 36% of sugar transporter genes were differentially expressed. Several of them, such as GLUTs, TPTs, and aquaporins, with glucose, triose-phosphate sugars, and glycerol as potential substrates, were upregulated at the holobiont and community level. We also showed that algal sugar transporter genes exhibit distinct temporal expression patterns during the day. This reprogrammed transportome indicates that symbiosis has a major impact on sugar fluxes within and outside the algal cell, and highlights the complexity and the dynamics of metabolic exchanges between partners. This study improves our understanding of the molecular players of the metabolic connectivity underlying the ecological success of planktonic photosymbiosis and paves the way for more studies on transporters across photosymbiotic models.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"21 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2024-12-09","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142805442","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}
María Dolores Ramos-Barbero, Borja Aldeguer-Riquelme, Tomeu Viver, Judith Villamor, Miryam Carrillo-Bautista, Cristina López-Pascual, Konstantinos T Konstantinidis, Manuel Martínez-García, Fernando Santos, Ramon Rossello-Mora, Josefa Antón
Viruses shape microbial community structure and activity through the control of population diversity and cell abundances. Identifying and monitoring the dynamics of specific virus-host pairs in nature is hampered by the limitations of culture-independent approaches such as metagenomics, which do not always provide strain-level resolution, and culture-based analyses, which eliminate the ecological background and in-situ interactions. Here, we have explored the interaction of a specific “autochthonous” host strain and its viruses within a natural community. Bacterium Salinibacter ruber strain M8 was spiked into its environment of isolation, a crystallizer pond from a coastal saltern, and the viral and cellular communities were monitored for one month using culture, metagenomics, and microscopy. Metagenome sequencing indicated that the M8 abundance decreased sharply after being added to the pond, likely due to forces other than viral predation. However, the presence of M8 selected for two species of a new viral genus, Phoenicisalinivirus, for which 120 strains were isolated. During this experiment, an assemblage of closely related viral genomic variants was replaced by a single population with the ability to infect M8, a scenario which was compatible with the selection of a genomic variant from the rare biosphere. Further analysis implicated a viral genomic region putatively coding for a tail fiber protein to be responsible for M8 specificity. Our results indicate that low abundance viral genotypes provide a viral seed bank that allows for a highly specialized virus-host response within a complex ecological background.
{"title":"Experimental evolution at ecological scales allows linking of viral genotypes to specific host strains","authors":"María Dolores Ramos-Barbero, Borja Aldeguer-Riquelme, Tomeu Viver, Judith Villamor, Miryam Carrillo-Bautista, Cristina López-Pascual, Konstantinos T Konstantinidis, Manuel Martínez-García, Fernando Santos, Ramon Rossello-Mora, Josefa Antón","doi":"10.1093/ismejo/wrae208","DOIUrl":"https://doi.org/10.1093/ismejo/wrae208","url":null,"abstract":"Viruses shape microbial community structure and activity through the control of population diversity and cell abundances. Identifying and monitoring the dynamics of specific virus-host pairs in nature is hampered by the limitations of culture-independent approaches such as metagenomics, which do not always provide strain-level resolution, and culture-based analyses, which eliminate the ecological background and in-situ interactions. Here, we have explored the interaction of a specific “autochthonous” host strain and its viruses within a natural community. Bacterium Salinibacter ruber strain M8 was spiked into its environment of isolation, a crystallizer pond from a coastal saltern, and the viral and cellular communities were monitored for one month using culture, metagenomics, and microscopy. Metagenome sequencing indicated that the M8 abundance decreased sharply after being added to the pond, likely due to forces other than viral predation. However, the presence of M8 selected for two species of a new viral genus, Phoenicisalinivirus, for which 120 strains were isolated. During this experiment, an assemblage of closely related viral genomic variants was replaced by a single population with the ability to infect M8, a scenario which was compatible with the selection of a genomic variant from the rare biosphere. Further analysis implicated a viral genomic region putatively coding for a tail fiber protein to be responsible for M8 specificity. Our results indicate that low abundance viral genotypes provide a viral seed bank that allows for a highly specialized virus-host response within a complex ecological background.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"5 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2024-11-23","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142694181","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}
Rasit Asiloglu, Seda Ozer Bodur, Solomon Oloruntoba Samuel, Murat Aycan, Jun Murase, Naoki Harada
The plant-microbe interactions, which is crucial for plant health and productivity, mainly occur in rhizosphere: a narrow zone of soil surrounding roots of living plants. The rhizosphere hosts one of the most intense habitats for microbial prey–predator interactions, especially between predatory protists and bacteria. Here, based on two key facts, microbial predators modulate rhizobacterial community composition, and the rhizobacterial community is the primary source of root microbiome, endophytes; we hypothesized that predation upon rhizobacteria would modulate the community composition of endophytic bacteria. The effects of three taxonomically distinct axenic protist species (Acanthamoeba castellanii, Vermamoeba vermiformis, and Heteromita globosa) were tested in this study. To examine the robustness of the hypotheses, the experiments were conducted in three soil types characterized by distinct bacterial communities and physicochemical properties. The bacterial community compositions were analyzed with high throughput sequencing. Bacterial gene abundances were estimated with a real-time-PCR method. The results showed that protists modulated endophytic communities, which originated in the rhizosphere soil. The modulation of endophytic communities by protists showed chaotic patterns rather than a deterministic effect under different soil types. The observed chaotic dynamics were further confirmed with an additional experiment, in which chaos was triggered by changes in the dilution rates of soil nutrients. Furthermore, the presence of predators enhanced the root colonization of endophytes. Our findings identify a key mechanism for the modulation of root endophytes and enhance understanding of underground plant-microbe interactions, which can lead to open new avenues for modulating the root microbiome to enhance crop production.
{"title":"Trophic modulation of endophytes by rhizosphere protists","authors":"Rasit Asiloglu, Seda Ozer Bodur, Solomon Oloruntoba Samuel, Murat Aycan, Jun Murase, Naoki Harada","doi":"10.1093/ismejo/wrae235","DOIUrl":"https://doi.org/10.1093/ismejo/wrae235","url":null,"abstract":"The plant-microbe interactions, which is crucial for plant health and productivity, mainly occur in rhizosphere: a narrow zone of soil surrounding roots of living plants. The rhizosphere hosts one of the most intense habitats for microbial prey–predator interactions, especially between predatory protists and bacteria. Here, based on two key facts, microbial predators modulate rhizobacterial community composition, and the rhizobacterial community is the primary source of root microbiome, endophytes; we hypothesized that predation upon rhizobacteria would modulate the community composition of endophytic bacteria. The effects of three taxonomically distinct axenic protist species (Acanthamoeba castellanii, Vermamoeba vermiformis, and Heteromita globosa) were tested in this study. To examine the robustness of the hypotheses, the experiments were conducted in three soil types characterized by distinct bacterial communities and physicochemical properties. The bacterial community compositions were analyzed with high throughput sequencing. Bacterial gene abundances were estimated with a real-time-PCR method. The results showed that protists modulated endophytic communities, which originated in the rhizosphere soil. The modulation of endophytic communities by protists showed chaotic patterns rather than a deterministic effect under different soil types. The observed chaotic dynamics were further confirmed with an additional experiment, in which chaos was triggered by changes in the dilution rates of soil nutrients. Furthermore, the presence of predators enhanced the root colonization of endophytes. Our findings identify a key mechanism for the modulation of root endophytes and enhance understanding of underground plant-microbe interactions, which can lead to open new avenues for modulating the root microbiome to enhance crop production.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"6 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2024-11-20","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142678496","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}
Joaquín Martínez Martínez, David Talmy, Jeffrey A Kimbrel, Peter K Weber, Xavier Mayali
Free viruses are the most abundant type of biological particles in the biosphere, but the lack of quantitative knowledge about their consumption by heterotrophic protists and bacterial degradation has hindered the inclusion of virovory in biogeochemical models. Using isotope-labeled viruses added to three independent microcosm experiments with natural microbial communities followed by isotope measurements with single-cell resolution and flow cytometry, we quantified the flux of viral C and N into virovorous protists and bacteria and compared the loss of viruses due to abiotic vs biotic factors. We found that some protists can obtain most of their C and N requirements from viral particles and that viral C and N get incorporated into bacterial biomass. We found that bacteria and protists were responsible for increasing the daily removal rate of viruses by 33% to 85%, respectively, compared to abiotic processes alone. Our laboratory incubation experiments showed that abiotic processes removed roughly 50% of the viruses within a week, and adding biotic processes led to a removal of 83% to 91%. Our data provide direct evidence for the transfer of viral C and N back into the microbial loop through protist grazing and bacterial breakdown, representing a globally significant flux that needs to be investigated further to better understand and predictably model the C and N cycles of the hydrosphere.
游离病毒是生物圈中最丰富的生物颗粒类型，但由于缺乏有关异养原生生物消耗病毒和细菌降解病毒的定量知识，将病毒纳入生物地球化学模型的工作受到了阻碍。通过在三个独立的自然微生物群落微宇宙实验中添加同位素标记的病毒，然后利用单细胞分辨率和流式细胞仪进行同位素测量，我们量化了病毒 C 和 N 进入食病毒原生动物和细菌的通量，并比较了非生物因素和生物因素造成的病毒损失。我们发现，一些原生动物可以从病毒颗粒中获得其所需的大部分 C 和 N，而病毒 C 和 N 则会融入细菌的生物量中。我们发现，与单独的非生物过程相比，细菌和原生生物可使病毒的日清除率分别提高 33% 至 85%。我们的实验室培养实验表明，非生物过程在一周内清除了大约 50%的病毒，而加入生物过程后，病毒清除率提高了 83% 至 91%。我们的数据提供了直接证据，证明病毒的碳和氮通过原生动物的捕食和细菌的分解又回到了微生物循环中，这是一个全球性的重要通量，需要进一步研究，以更好地理解和预测水圈的碳和氮循环模型。
{"title":"Coastal bacteria and protists assimilate viral carbon and nitrogen","authors":"Joaquín Martínez Martínez, David Talmy, Jeffrey A Kimbrel, Peter K Weber, Xavier Mayali","doi":"10.1093/ismejo/wrae231","DOIUrl":"https://doi.org/10.1093/ismejo/wrae231","url":null,"abstract":"Free viruses are the most abundant type of biological particles in the biosphere, but the lack of quantitative knowledge about their consumption by heterotrophic protists and bacterial degradation has hindered the inclusion of virovory in biogeochemical models. Using isotope-labeled viruses added to three independent microcosm experiments with natural microbial communities followed by isotope measurements with single-cell resolution and flow cytometry, we quantified the flux of viral C and N into virovorous protists and bacteria and compared the loss of viruses due to abiotic vs biotic factors. We found that some protists can obtain most of their C and N requirements from viral particles and that viral C and N get incorporated into bacterial biomass. We found that bacteria and protists were responsible for increasing the daily removal rate of viruses by 33% to 85%, respectively, compared to abiotic processes alone. Our laboratory incubation experiments showed that abiotic processes removed roughly 50% of the viruses within a week, and adding biotic processes led to a removal of 83% to 91%. Our data provide direct evidence for the transfer of viral C and N back into the microbial loop through protist grazing and bacterial breakdown, representing a globally significant flux that needs to be investigated further to better understand and predictably model the C and N cycles of the hydrosphere.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"11 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2024-11-13","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142610260","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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