Lingrui Qu, Chao Wang, Stefano Manzoni, Marina Dacal, Fernando T Maestre, Edith Bai
Ongoing global warming is expected to augment soil respiration by increasing microbial activity, driving self-reinforcing feedback to climate change. However, the compensatory thermal adaptation of soil microorganisms and substrate depletion may weaken the effects of rising temperature on soil respiration. To test this hypothesis, we collected soils along a large-scale forest transect in eastern China spanning a natural temperature gradient, and incubated the soils at different temperatures with or without substrate addition. We combined the exponential thermal response function and a data-driven model to study the interaction effect of thermal adaptation and substrate availability on microbial respiration and compared our results to those from two additional continental and global independent datasets. Modelled results suggested that the effect of thermal adaptation on microbial respiration was greater in areas with higher mean annual temperatures, consistent with the compensatory response to warming. In addition, the effect of thermal adaptation on microbial respiration was greater under substrate addition than under substrate depletion, which was also true for the independent datasets reanalyzed using our approach. Our results indicate that thermal adaptation in warmer regions could exert a more pronounced negative impact on microbial respiration when substrate availability is abundant. These findings improve the body of knowledge on how substrate availability influences soil microbial community-temperature interactions, which could improve estimates of projected soil carbon losses to the atmosphere through respiration.
{"title":"Stronger compensatory thermal adaptation of soil microbial respiration with higher substrate availability","authors":"Lingrui Qu, Chao Wang, Stefano Manzoni, Marina Dacal, Fernando T Maestre, Edith Bai","doi":"10.1093/ismejo/wrae025","DOIUrl":"https://doi.org/10.1093/ismejo/wrae025","url":null,"abstract":"Ongoing global warming is expected to augment soil respiration by increasing microbial activity, driving self-reinforcing feedback to climate change. However, the compensatory thermal adaptation of soil microorganisms and substrate depletion may weaken the effects of rising temperature on soil respiration. To test this hypothesis, we collected soils along a large-scale forest transect in eastern China spanning a natural temperature gradient, and incubated the soils at different temperatures with or without substrate addition. We combined the exponential thermal response function and a data-driven model to study the interaction effect of thermal adaptation and substrate availability on microbial respiration and compared our results to those from two additional continental and global independent datasets. Modelled results suggested that the effect of thermal adaptation on microbial respiration was greater in areas with higher mean annual temperatures, consistent with the compensatory response to warming. In addition, the effect of thermal adaptation on microbial respiration was greater under substrate addition than under substrate depletion, which was also true for the independent datasets reanalyzed using our approach. Our results indicate that thermal adaptation in warmer regions could exert a more pronounced negative impact on microbial respiration when substrate availability is abundant. These findings improve the body of knowledge on how substrate availability influences soil microbial community-temperature interactions, which could improve estimates of projected soil carbon losses to the atmosphere through respiration.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":null,"pages":null},"PeriodicalIF":0.0,"publicationDate":"2024-02-12","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"139728099","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}
Isabella T Ritchie, Brayan Vilanova-Cuevas, Ashley Altera, Kaileigh Cornfield, Ceri Evans, James S Evans, Maria Hopson-Fernandes, Christina A Kellogg, Elayne Looker, Oliver Taylor, Ian Hewson, Mya Breitbart
Mass mortality of the dominant coral reef herbivore Diadema antillarum in the Caribbean in the early 1980s led to a persistent phase shift from coral- to algal-dominated reefs. In 2022, a scuticociliate most closely related to Philaster apodigitiformis caused further mass mortality of D. antillarum across the Caribbean, leading to >95% mortality at affected sites. Mortality was also reported in the related species Diadema setosum in the Mediterranean in 2022, where urchins experienced gross signs compatible with scuticociliatosis. However, the causative agent of the Mediterranean outbreak has not yet been determined. In April 2023, mass mortality of D. setosum occurred along the Sultanate of Oman’s coastline. Urchins displayed signs compatible with scuticociliatosis including abnormal behavior, drooping and loss of spines, followed by tissue necrosis and death. Here we report the detection of an 18S rRNA gene sequence in abnormal urchins from Muscat, Oman that is identical to the Philaster strain responsible for D. antillarum mass mortality in the Caribbean. We also show that scuticociliatosis signs can be elicited in D. setosum by experimental challenge with the cultivated Philaster strain associated with Caribbean scuticociliatosis. These results demonstrate the Philaster sp. associated with D. antillarum mass mortality has rapidly spread to geographically distant coral reefs, compelling global-scale awareness and monitoring for this devastating condition through field surveys, microscopy, and molecular microbiological approaches, and prompting investigation of long-range transmission mechanisms.
{"title":"Transglobal spread of an ecologically relevant sea urchin parasite","authors":"Isabella T Ritchie, Brayan Vilanova-Cuevas, Ashley Altera, Kaileigh Cornfield, Ceri Evans, James S Evans, Maria Hopson-Fernandes, Christina A Kellogg, Elayne Looker, Oliver Taylor, Ian Hewson, Mya Breitbart","doi":"10.1093/ismejo/wrae024","DOIUrl":"https://doi.org/10.1093/ismejo/wrae024","url":null,"abstract":"Mass mortality of the dominant coral reef herbivore Diadema antillarum in the Caribbean in the early 1980s led to a persistent phase shift from coral- to algal-dominated reefs. In 2022, a scuticociliate most closely related to Philaster apodigitiformis caused further mass mortality of D. antillarum across the Caribbean, leading to >95% mortality at affected sites. Mortality was also reported in the related species Diadema setosum in the Mediterranean in 2022, where urchins experienced gross signs compatible with scuticociliatosis. However, the causative agent of the Mediterranean outbreak has not yet been determined. In April 2023, mass mortality of D. setosum occurred along the Sultanate of Oman’s coastline. Urchins displayed signs compatible with scuticociliatosis including abnormal behavior, drooping and loss of spines, followed by tissue necrosis and death. Here we report the detection of an 18S rRNA gene sequence in abnormal urchins from Muscat, Oman that is identical to the Philaster strain responsible for D. antillarum mass mortality in the Caribbean. We also show that scuticociliatosis signs can be elicited in D. setosum by experimental challenge with the cultivated Philaster strain associated with Caribbean scuticociliatosis. These results demonstrate the Philaster sp. associated with D. antillarum mass mortality has rapidly spread to geographically distant coral reefs, compelling global-scale awareness and monitoring for this devastating condition through field surveys, microscopy, and molecular microbiological approaches, and prompting investigation of long-range transmission mechanisms.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":null,"pages":null},"PeriodicalIF":0.0,"publicationDate":"2024-02-08","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"139716983","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}
Mira D Liu, Yongle Du, Sara K Koupaei, Nicole R Kim, Monika S Fischer, Wenjun Zhang, Matthew F Traxler
Wildfires affect soils in multiple ways, leading to numerous challenges for colonizing microorganisms. While it is thought that fire-adapted microorganisms lie at the forefront of postfire ecosystem recovery, the specific strategies that these organisms use to thrive in burned soils remain largely unknown. Through bioactivity screening of bacterial isolates from burned soils, we discovered that several Paraburkholderia spp. isolates produced a set of unusual rhamnolipid surfactants with a natural methyl ester modification. These rhamnolipid methyl esters (RLMEs) exhibited enhanced antimicrobial activity against other postfire microbial isolates, including pyrophilous Pyronema fungi and Amycolatopsis bacteria, compared to the typical rhamnolipids made by organisms such as Pseudomonas spp. RLMEs also showed enhanced surfactant properties and facilitated bacterial motility on agar surfaces. In vitro assays further demonstrated that RLMEs improved aqueous solubilization of polycyclic aromatic hydrocarbons, which are potential carbon sources found in char. Identification of the rhamnolipid biosynthesis genes in the postfire isolate, Paraburkholderia kirstenboschensis str. F3, led to the discovery of rhlM, whose gene product is responsible for the unique methylation of rhamnolipid substrates. RhlM is the first characterized bacterial representative of a large class of integral membrane methyltransferases that are widespread in bacteria. These results indicate multiple roles for RLMEs in the postfire lifestyle of Paraburkholderia isolates, including enhanced dispersal, solubilization of potential nutrients, and inhibition of competitors. Our findings shed new light on the chemical adaptations that bacteria employ to navigate, grow, and outcompete other soil community members in postfire environments.
{"title":"Surface-active antibiotic production as a multifunctional adaptation for postfire microorganisms","authors":"Mira D Liu, Yongle Du, Sara K Koupaei, Nicole R Kim, Monika S Fischer, Wenjun Zhang, Matthew F Traxler","doi":"10.1093/ismejo/wrae022","DOIUrl":"https://doi.org/10.1093/ismejo/wrae022","url":null,"abstract":"Wildfires affect soils in multiple ways, leading to numerous challenges for colonizing microorganisms. While it is thought that fire-adapted microorganisms lie at the forefront of postfire ecosystem recovery, the specific strategies that these organisms use to thrive in burned soils remain largely unknown. Through bioactivity screening of bacterial isolates from burned soils, we discovered that several Paraburkholderia spp. isolates produced a set of unusual rhamnolipid surfactants with a natural methyl ester modification. These rhamnolipid methyl esters (RLMEs) exhibited enhanced antimicrobial activity against other postfire microbial isolates, including pyrophilous Pyronema fungi and Amycolatopsis bacteria, compared to the typical rhamnolipids made by organisms such as Pseudomonas spp. RLMEs also showed enhanced surfactant properties and facilitated bacterial motility on agar surfaces. In vitro assays further demonstrated that RLMEs improved aqueous solubilization of polycyclic aromatic hydrocarbons, which are potential carbon sources found in char. Identification of the rhamnolipid biosynthesis genes in the postfire isolate, Paraburkholderia kirstenboschensis str. F3, led to the discovery of rhlM, whose gene product is responsible for the unique methylation of rhamnolipid substrates. RhlM is the first characterized bacterial representative of a large class of integral membrane methyltransferases that are widespread in bacteria. These results indicate multiple roles for RLMEs in the postfire lifestyle of Paraburkholderia isolates, including enhanced dispersal, solubilization of potential nutrients, and inhibition of competitors. Our findings shed new light on the chemical adaptations that bacteria employ to navigate, grow, and outcompete other soil community members in postfire environments.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":null,"pages":null},"PeriodicalIF":0.0,"publicationDate":"2024-02-05","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"139700852","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}
Ana Popovic, Eric Yixiao Cao, Joanna Han, Nirvana Nursimulu, Eliza V C Alves-Ferreira, Kyle Burrows, Andrea Kennard, Noor Alsmadi, Michael E Grigg, Arthur Mortha, John Parkinson
Commensal protists and gut bacterial communities exhibit complex relationships, mediated at least in part through host immunity. To improve our understanding of this tripartite interplay, we investigated community and functional dynamics between the murine protist Tritrichomonas musculus (Tmu) and intestinal bacteria in healthy and B cell-deficient mice. We identified dramatic, protist-driven remodeling of resident microbiome growth and activities, in parallel with Tmu functional changes, which were accelerated in the absence of B cells. Metatranscriptomic data revealed nutrient-based competition between bacteria and the protist. Single cell transcriptomics identified distinct Tmu life stages, providing new evidence for trichomonad sexual replication and the formation of pseudocysts. Unique cell states were validated in situ through microscopy and flow cytometry. Our results reveal complex microbial dynamics during the establishment of a commensal protist in the gut, and provide valuable datasets to drive future mechanistic studies.
共生原生动物和肠道细菌群落之间的关系很复杂，至少部分是通过宿主免疫力来调节的。为了加深我们对这种三方相互作用的理解，我们研究了健康小鼠和 B 细胞缺陷小鼠体内小鼠原生动物麝香蓟马（Tritrichomonas musculus，Tmu）与肠道细菌之间的群落和功能动态。我们发现了原生动物驱动的常驻微生物群生长和活动的巨大重塑，与此同时，Tmu 的功能也发生了变化，在缺乏 B 细胞的情况下，这种变化会加速。元转录组数据揭示了细菌与原生动物之间基于营养的竞争。单细胞转录组学确定了不同的 Tmu 生命阶段，为滴虫的有性复制和假囊的形成提供了新的证据。通过显微镜和流式细胞术对独特的细胞状态进行了原位验证。我们的研究结果揭示了一种共生原生动物在肠道建立过程中复杂的微生物动态，并为推动未来的机理研究提供了宝贵的数据集。
{"title":"Commensal protist Tritrichomonas musculus exhibits a dynamic life cycle that induces extensive remodeling of the gut microbiota","authors":"Ana Popovic, Eric Yixiao Cao, Joanna Han, Nirvana Nursimulu, Eliza V C Alves-Ferreira, Kyle Burrows, Andrea Kennard, Noor Alsmadi, Michael E Grigg, Arthur Mortha, John Parkinson","doi":"10.1093/ismejo/wrae023","DOIUrl":"https://doi.org/10.1093/ismejo/wrae023","url":null,"abstract":"Commensal protists and gut bacterial communities exhibit complex relationships, mediated at least in part through host immunity. To improve our understanding of this tripartite interplay, we investigated community and functional dynamics between the murine protist Tritrichomonas musculus (Tmu) and intestinal bacteria in healthy and B cell-deficient mice. We identified dramatic, protist-driven remodeling of resident microbiome growth and activities, in parallel with Tmu functional changes, which were accelerated in the absence of B cells. Metatranscriptomic data revealed nutrient-based competition between bacteria and the protist. Single cell transcriptomics identified distinct Tmu life stages, providing new evidence for trichomonad sexual replication and the formation of pseudocysts. Unique cell states were validated in situ through microscopy and flow cytometry. Our results reveal complex microbial dynamics during the establishment of a commensal protist in the gut, and provide valuable datasets to drive future mechanistic studies.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":null,"pages":null},"PeriodicalIF":0.0,"publicationDate":"2024-02-02","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"139700815","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}
Huaming Wu, Xingqiang Wu, Lorenzo Rovelli, Andreas Lorke
Prediction of the complex cyanobacteria-environment interactions is vital for understanding harmful bloom formation. Most previous studies on these interactions considered specific properties of cyanobacterial cells as representative for the entire population (e.g., growth rate, mortality, and photosynthetic capacity (Pmax)), and assumed that they remained spatiotemporally unchanged. Although, at the population level, the alteration of such traits can be driven by intraspecific competition, little is known about how traits and their plasticity change in response to environmental conditions and affect the bloom formation. Here we test the hypothesis that intraspecific variations in Pmax of cyanobacteria (Microcystis spp.) play an important role in its population dynamics. We coupled a one-dimensional hydrodynamic model with a trait-based phytoplankton model to simulate the effects of physical drivers (turbulence and turbidity) on the Pmax of Microcystis populations for a range of dynamic conditions typical for shallow eutrophic lakes. Our results revealed that turbulence acts as a directional selective driver for changes in Pmax. Depending on the intensity of daily-periodic turbulence, representing wind-driven mixing, a shift in population-averaged phenotypes occurred toward either low Pmax, allowing the population to capture additional light in the upper layers, or high Pmax, enhancing the efficiency of light utilization. Moreover, we observed that a high intraspecific diversity in Pmax accelerated the formation of surface scum by up to more than four times compared to a lower diversity. This study offers insights into mechanisms by which cyanobacteria populations respond to turbulence and underscores the significance of intraspecific variations in cyanobacterial bloom formation. Highlights
{"title":"Selection of photosynthetic traits by turbulent mixing governs formation of cyanobacterial blooms in shallow eutrophic lakes","authors":"Huaming Wu, Xingqiang Wu, Lorenzo Rovelli, Andreas Lorke","doi":"10.1093/ismejo/wrae021","DOIUrl":"https://doi.org/10.1093/ismejo/wrae021","url":null,"abstract":"Prediction of the complex cyanobacteria-environment interactions is vital for understanding harmful bloom formation. Most previous studies on these interactions considered specific properties of cyanobacterial cells as representative for the entire population (e.g., growth rate, mortality, and photosynthetic capacity (Pmax)), and assumed that they remained spatiotemporally unchanged. Although, at the population level, the alteration of such traits can be driven by intraspecific competition, little is known about how traits and their plasticity change in response to environmental conditions and affect the bloom formation. Here we test the hypothesis that intraspecific variations in Pmax of cyanobacteria (Microcystis spp.) play an important role in its population dynamics. We coupled a one-dimensional hydrodynamic model with a trait-based phytoplankton model to simulate the effects of physical drivers (turbulence and turbidity) on the Pmax of Microcystis populations for a range of dynamic conditions typical for shallow eutrophic lakes. Our results revealed that turbulence acts as a directional selective driver for changes in Pmax. Depending on the intensity of daily-periodic turbulence, representing wind-driven mixing, a shift in population-averaged phenotypes occurred toward either low Pmax, allowing the population to capture additional light in the upper layers, or high Pmax, enhancing the efficiency of light utilization. Moreover, we observed that a high intraspecific diversity in Pmax accelerated the formation of surface scum by up to more than four times compared to a lower diversity. This study offers insights into mechanisms by which cyanobacteria populations respond to turbulence and underscores the significance of intraspecific variations in cyanobacterial bloom formation. Highlights","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":null,"pages":null},"PeriodicalIF":0.0,"publicationDate":"2024-02-02","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"139676879","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}
Elias Broman, Markus Olsson, Adele Maciute, Daniel Donald, Christoph Humborg, Alf Norkko, Tom Jilbert, Stefano Bonaglia, Francisco J A Nascimento
Coastal ecosystems dominate oceanic methane (CH4) emissions. However, there is limited knowledge about how biotic interactions between infauna and aerobic methanotrophs (i.e. CH4 oxidizing bacteria) drive the spatial–temporal dynamics of these emissions. Here, we investigated the role of meio- and macrofauna in mediating CH4 sediment–water fluxes and aerobic methanotrophic activity that can oxidize significant portions of CH4. We show that macrofauna increases CH4 fluxes by enhancing vertical solute transport through bioturbation, but this effect is somewhat offset by high meiofauna abundance. The increase in CH4 flux reduces CH4 pore-water availability, resulting in lower abundance and activity of aerobic methanotrophs, an effect that counterbalances the potential stimulation of these bacteria by higher oxygen flux to the sediment via bioturbation. These findings indicate that a larger than previously thought portion of CH4 emissions from coastal ecosystems is due to faunal activity and multiple complex interactions with methanotrophs.
{"title":"Biotic interactions between benthic infauna and aerobic methanotrophs mediate methane fluxes from coastal sediments","authors":"Elias Broman, Markus Olsson, Adele Maciute, Daniel Donald, Christoph Humborg, Alf Norkko, Tom Jilbert, Stefano Bonaglia, Francisco J A Nascimento","doi":"10.1093/ismejo/wrae013","DOIUrl":"https://doi.org/10.1093/ismejo/wrae013","url":null,"abstract":"Coastal ecosystems dominate oceanic methane (CH4) emissions. However, there is limited knowledge about how biotic interactions between infauna and aerobic methanotrophs (i.e. CH4 oxidizing bacteria) drive the spatial–temporal dynamics of these emissions. Here, we investigated the role of meio- and macrofauna in mediating CH4 sediment–water fluxes and aerobic methanotrophic activity that can oxidize significant portions of CH4. We show that macrofauna increases CH4 fluxes by enhancing vertical solute transport through bioturbation, but this effect is somewhat offset by high meiofauna abundance. The increase in CH4 flux reduces CH4 pore-water availability, resulting in lower abundance and activity of aerobic methanotrophs, an effect that counterbalances the potential stimulation of these bacteria by higher oxygen flux to the sediment via bioturbation. These findings indicate that a larger than previously thought portion of CH4 emissions from coastal ecosystems is due to faunal activity and multiple complex interactions with methanotrophs.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":null,"pages":null},"PeriodicalIF":0.0,"publicationDate":"2024-02-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"139660138","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}
Esther Rubio-Portillo, Sophia Robertson, Josefa Antón
The increasing trend in sea surface temperature promotes the spread of Vibrio species, which are known to cause diseases in a wide range of marine organisms. Among these pathogens, Vibrio mediterranei has emerged as a significant threat, leading to bleaching in the coral species Oculina patagonica. Bacteriophages, or phages, are viruses that infect bacteria, thereby regulating microbial communities and playing a crucial role in the coral’s defense against pathogens. However, our understanding of phages that infect V. mediterranei is limited. In this study, we identified two phage species capable of infecting V. mediterranei, utilizing a combination of cultivation and metagenomic approaches. These phages are low-abundance specialists within the coral mucus layer that exhibit rapid proliferation in the presence of their hosts, suggesting a potential role in coral defense. Additionally, one of these phages possesses a conserved domain of a leucine-rich repeat protein, similar to those harbored in the coral genome, that plays a key role in pathogen recognition, hinting at potential coral-phage coevolution. Furthermore, our research suggests that lytic Vibrio infections could trigger prophage induction, which may disseminate genetic elements, including virulence factors, in the coral mucus layer. Overall, our findings underscore the importance of historical coral-phage interactions as a form of coral immunity against invasive Vibrio pathogens.
{"title":"Coral mucus as a reservoir of bacteriophages targeting Vibrio pathogens","authors":"Esther Rubio-Portillo, Sophia Robertson, Josefa Antón","doi":"10.1093/ismejo/wrae017","DOIUrl":"https://doi.org/10.1093/ismejo/wrae017","url":null,"abstract":"The increasing trend in sea surface temperature promotes the spread of Vibrio species, which are known to cause diseases in a wide range of marine organisms. Among these pathogens, Vibrio mediterranei has emerged as a significant threat, leading to bleaching in the coral species Oculina patagonica. Bacteriophages, or phages, are viruses that infect bacteria, thereby regulating microbial communities and playing a crucial role in the coral’s defense against pathogens. However, our understanding of phages that infect V. mediterranei is limited. In this study, we identified two phage species capable of infecting V. mediterranei, utilizing a combination of cultivation and metagenomic approaches. These phages are low-abundance specialists within the coral mucus layer that exhibit rapid proliferation in the presence of their hosts, suggesting a potential role in coral defense. Additionally, one of these phages possesses a conserved domain of a leucine-rich repeat protein, similar to those harbored in the coral genome, that plays a key role in pathogen recognition, hinting at potential coral-phage coevolution. Furthermore, our research suggests that lytic Vibrio infections could trigger prophage induction, which may disseminate genetic elements, including virulence factors, in the coral mucus layer. Overall, our findings underscore the importance of historical coral-phage interactions as a form of coral immunity against invasive Vibrio pathogens.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":null,"pages":null},"PeriodicalIF":0.0,"publicationDate":"2024-02-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"139660092","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}
Nan Yang, Henriette L Røder, Wisnu Adi Wicaksono, Birgit Wassermann, Jakob Russel, Xuanji Li, Joseph Nesme, Gabriele Berg, Søren J Sørensen, Mette Burmølle
Microorganisms colonizing plant roots co-exist in complex, spatially structured multispecies biofilm communities. However, little is known about microbial interactions and the underlying spatial organization within biofilm communities established on plant roots. Here, a well-established four-species biofilm model (Stenotrophomonas rhizophila, Paenibacillus amylolyticus, Microbacterium oxydans and Xanthomonas retroflexus, termed as SPMX) was applied to Arabidopsis roots to study the impact of multispecies biofilm on plant growth and the community spatial dynamics on the roots. SPMX co-culture notably promoted root development and plant biomass. Co-cultured SPMX increased root colonization and formed multispecies biofilms, structurally different from those formed by monocultures. By combining 16S rRNA gene amplicon sequencing and fluorescence in situ hybridization with confocal laser scanning microscopy (FISH-CLSM), we found that the composition and spatial organization of the four-species biofilm significantly changed over time. Monoculture P. amylolyticus colonized plant roots poorly, but its population and root colonization were highly enhanced when residing in the four-species biofilm. Exclusion of P. amylolyticus from the community reduced overall biofilm production and root colonization of the three species, resulting in the loss of the plant growth-promoting effects. Combined with spatial analysis, this led to identification of P. amylolyticus as a keystone species. Our findings highlight that weak root colonizers may benefit from mutualistic interactions in complex communities and hereby become important keystone species impacting community spatial organization and function. This work expands the knowledge on spatial organization uncovering interspecific interactions in multispecies biofilm communities on plant roots, beneficial for harnessing microbial mutualism promoting plant growth.
{"title":"Interspecific interactions facilitate keystone species in a multispecies biofilm that promotes plant growth","authors":"Nan Yang, Henriette L Røder, Wisnu Adi Wicaksono, Birgit Wassermann, Jakob Russel, Xuanji Li, Joseph Nesme, Gabriele Berg, Søren J Sørensen, Mette Burmølle","doi":"10.1093/ismejo/wrae012","DOIUrl":"https://doi.org/10.1093/ismejo/wrae012","url":null,"abstract":"Microorganisms colonizing plant roots co-exist in complex, spatially structured multispecies biofilm communities. However, little is known about microbial interactions and the underlying spatial organization within biofilm communities established on plant roots. Here, a well-established four-species biofilm model (Stenotrophomonas rhizophila, Paenibacillus amylolyticus, Microbacterium oxydans and Xanthomonas retroflexus, termed as SPMX) was applied to Arabidopsis roots to study the impact of multispecies biofilm on plant growth and the community spatial dynamics on the roots. SPMX co-culture notably promoted root development and plant biomass. Co-cultured SPMX increased root colonization and formed multispecies biofilms, structurally different from those formed by monocultures. By combining 16S rRNA gene amplicon sequencing and fluorescence in situ hybridization with confocal laser scanning microscopy (FISH-CLSM), we found that the composition and spatial organization of the four-species biofilm significantly changed over time. Monoculture P. amylolyticus colonized plant roots poorly, but its population and root colonization were highly enhanced when residing in the four-species biofilm. Exclusion of P. amylolyticus from the community reduced overall biofilm production and root colonization of the three species, resulting in the loss of the plant growth-promoting effects. Combined with spatial analysis, this led to identification of P. amylolyticus as a keystone species. Our findings highlight that weak root colonizers may benefit from mutualistic interactions in complex communities and hereby become important keystone species impacting community spatial organization and function. This work expands the knowledge on spatial organization uncovering interspecific interactions in multispecies biofilm communities on plant roots, beneficial for harnessing microbial mutualism promoting plant growth.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":null,"pages":null},"PeriodicalIF":0.0,"publicationDate":"2024-01-29","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"139660175","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}
Samuel M McNichol, Fernando Sanchez-Quete, Stephanie K Loeb, Andreas Teske, Sunita R Shah Walter, Nagissa Mahmoudi
Growing evidence suggests that interactions among heterotrophic microorganisms influence the efficiency and rate of organic matter turnover. These interactions are dynamic and shaped by the composition and availability of resources in their surrounding environment. Heterotrophic microorganisms inhabiting marine environments often encounter fluctuations in the quality and quantity of carbon inputs, ranging from simple sugars to large, complex compounds. Here, we experimentally tested how the chemical complexity of carbon substrates affects competition and growth dynamics between two heterotrophic marine isolates. We tracked cell density using species-specific PCR assays and measured rates of microbial CO2 production along with associated isotopic signatures (13C and 14C) to quantify the impact of these interactions on organic matter remineralization. The observed cell densities revealed substrate-driven interactions: one species exhibited a competitive advantage and quickly outgrew the other when incubated with a labile compound whereas both species seemed to coexist harmoniously in the presence of more complex organic matter. Rates of CO2 respiration revealed that co-incubation of these isolates enhanced organic matter turnover, sometimes by nearly twofold, compared to their incubation as mono-cultures. Isotopic signatures of respired CO2 indicated that co-incubation resulted in a greater remineralization of macromolecular organic matter. These results demonstrate that simple substrates promote competition whereas high substrate complexity reduces competitiveness and promotes the partitioning of degradative activities into distinct niches, facilitating coordinated utilization of the carbon pool. Taken together, this study yields new insight into how the quality of organic matter plays a pivotal role in determining microbial interactions within marine environments.
{"title":"Dynamics of carbon substrate competition among heterotrophic microorganisms.","authors":"Samuel M McNichol, Fernando Sanchez-Quete, Stephanie K Loeb, Andreas Teske, Sunita R Shah Walter, Nagissa Mahmoudi","doi":"10.1093/ismejo/wrae018","DOIUrl":"https://doi.org/10.1093/ismejo/wrae018","url":null,"abstract":"Growing evidence suggests that interactions among heterotrophic microorganisms influence the efficiency and rate of organic matter turnover. These interactions are dynamic and shaped by the composition and availability of resources in their surrounding environment. Heterotrophic microorganisms inhabiting marine environments often encounter fluctuations in the quality and quantity of carbon inputs, ranging from simple sugars to large, complex compounds. Here, we experimentally tested how the chemical complexity of carbon substrates affects competition and growth dynamics between two heterotrophic marine isolates. We tracked cell density using species-specific PCR assays and measured rates of microbial CO2 production along with associated isotopic signatures (13C and 14C) to quantify the impact of these interactions on organic matter remineralization. The observed cell densities revealed substrate-driven interactions: one species exhibited a competitive advantage and quickly outgrew the other when incubated with a labile compound whereas both species seemed to coexist harmoniously in the presence of more complex organic matter. Rates of CO2 respiration revealed that co-incubation of these isolates enhanced organic matter turnover, sometimes by nearly twofold, compared to their incubation as mono-cultures. Isotopic signatures of respired CO2 indicated that co-incubation resulted in a greater remineralization of macromolecular organic matter. These results demonstrate that simple substrates promote competition whereas high substrate complexity reduces competitiveness and promotes the partitioning of degradative activities into distinct niches, facilitating coordinated utilization of the carbon pool. Taken together, this study yields new insight into how the quality of organic matter plays a pivotal role in determining microbial interactions within marine environments.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":null,"pages":null},"PeriodicalIF":0.0,"publicationDate":"2024-01-29","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"139577413","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}
Álvaro Morón, Alaa E Tarhouchi, Iván Belinchón, Juan M Valenzuela, Patricia de Francisco, Ana Martín-González, Francisco Amaro
Bacterivorous protists are thought to serve as training grounds for bacterial pathogens by subjecting them to the same hostile conditions that they will encounter in the human host. Bacteria that survive intracellular digestion exhibit enhanced virulence and stress resistance after successful passage through protozoa but the underlying mechanisms are unknown. Here we show that the opportunistic pathogen Burkholderia cenocepacia survives phagocytosis by ciliates found in domestic and hospital sink drains, and viable bacteria are expelled packaged in respirable membrane vesicles with enhanced resistance to oxidative stress, desiccation and antibiotics, thereby contributing to pathogen dissemination in the environment. Reactive oxygen species generated within the protozoan phagosome promote the formation of persisters tolerant to ciprofloxacin by activating the bacterial SOS response. In addition, we show that genes encoding antioxidant enzymes are upregulated during passage through ciliates increasing bacterial resistance to oxidative radicals. We prove that suppression of the SOS response impairs bacterial intracellular survival and persister formation within protists. This study highlights the significance of protozoan food vacuoles as niches that foster bacterial adaptation in natural and built environments and suggests that persister switch within phagosomes may be a widespread phenomenon in bacteria surviving intracellular digestion.
食菌性原生动物被认为是细菌病原体的训练场，让它们经受在人类宿主体内会遇到的敌对条件。成功通过原生动物后，在细胞内消化中存活下来的细菌会表现出更强的毒力和抗应激能力，但其潜在机制尚不清楚。在这里，我们展示了机会性病原体伯克霍尔德氏原虫（Burkholderia cenocepacia）在家庭和医院水槽排水沟中发现的纤毛虫的吞噬作用下存活下来，存活的细菌被包装在可呼吸膜囊泡中排出，对氧化应激、干燥和抗生素的抵抗力增强，从而促进了病原体在环境中的传播。原生动物吞噬体中产生的活性氧通过激活细菌的 SOS 反应，促进了对环丙沙星耐受性强的宿主的形成。此外，我们还发现，编码抗氧化酶的基因在通过纤毛虫时会上调，从而增强细菌对氧化自由基的抵抗力。我们证明，抑制 SOS 反应会损害细菌在原生动物体内的生存和宿主的形成。这项研究强调了原生动物食物空泡作为促进细菌适应自然和人造环境的龛位的重要性，并表明在吞噬体中的宿主转换可能是细菌在细胞内消化存活的普遍现象。
{"title":"Protozoan predation enhances stress resistance and antibiotic tolerance in Burkholderia cenocepacia by triggering the SOS response","authors":"Álvaro Morón, Alaa E Tarhouchi, Iván Belinchón, Juan M Valenzuela, Patricia de Francisco, Ana Martín-González, Francisco Amaro","doi":"10.1093/ismejo/wrae014","DOIUrl":"https://doi.org/10.1093/ismejo/wrae014","url":null,"abstract":"Bacterivorous protists are thought to serve as training grounds for bacterial pathogens by subjecting them to the same hostile conditions that they will encounter in the human host. Bacteria that survive intracellular digestion exhibit enhanced virulence and stress resistance after successful passage through protozoa but the underlying mechanisms are unknown. Here we show that the opportunistic pathogen Burkholderia cenocepacia survives phagocytosis by ciliates found in domestic and hospital sink drains, and viable bacteria are expelled packaged in respirable membrane vesicles with enhanced resistance to oxidative stress, desiccation and antibiotics, thereby contributing to pathogen dissemination in the environment. Reactive oxygen species generated within the protozoan phagosome promote the formation of persisters tolerant to ciprofloxacin by activating the bacterial SOS response. In addition, we show that genes encoding antioxidant enzymes are upregulated during passage through ciliates increasing bacterial resistance to oxidative radicals. We prove that suppression of the SOS response impairs bacterial intracellular survival and persister formation within protists. This study highlights the significance of protozoan food vacuoles as niches that foster bacterial adaptation in natural and built environments and suggests that persister switch within phagosomes may be a widespread phenomenon in bacteria surviving intracellular digestion.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":null,"pages":null},"PeriodicalIF":0.0,"publicationDate":"2024-01-28","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"139577385","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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