Hayley E Knights, Vinoy K Ramachandran, Beatriz Jorrin, Raphael Ledermann, Jack D Parsons, Samuel T N Aroney, Philip S Poole
Bacterial persistence in the rhizosphere and colonisation of root niches are critical for the establishment of many beneficial plant-bacteria interactions including those between Rhizobium leguminosarum and its host legumes. Despite this, most studies on R. leguminosarum have focused on its symbiotic lifestyle as an endosymbiont in root nodules. Here, we use random barcode transposon sequencing (RB-TnSeq) to assay gene contributions of R. leguminosarum during competitive growth in the rhizosphere and colonisation of various plant species. This facilitated the identification of 189 genes commonly required for growth in diverse plant rhizospheres, mutation of 111 of which also affected subsequent root colonisation (rhizosphere progressive), and a further 119 genes necessary for colonisation. Common determinants reveal a need to synthesise essential compounds (amino acids, ribonucleotides, and cofactors), adapt metabolic function, respond to external stimuli, and withstand various stresses (such as changes in osmolarity). Additionally, chemotaxis and flagella-mediated motility are prerequisites for root colonisation. Many genes showed plant-specific dependencies highlighting significant adaptation to different plant species. This work provides a greater understanding of factors promoting rhizosphere fitness and root colonisation in plant-beneficial bacteria, facilitating their exploitation for agricultural benefit.
{"title":"Rhizobium determinants of rhizosphere persistence and root colonisation","authors":"Hayley E Knights, Vinoy K Ramachandran, Beatriz Jorrin, Raphael Ledermann, Jack D Parsons, Samuel T N Aroney, Philip S Poole","doi":"10.1093/ismejo/wrae072","DOIUrl":"https://doi.org/10.1093/ismejo/wrae072","url":null,"abstract":"Bacterial persistence in the rhizosphere and colonisation of root niches are critical for the establishment of many beneficial plant-bacteria interactions including those between Rhizobium leguminosarum and its host legumes. Despite this, most studies on R. leguminosarum have focused on its symbiotic lifestyle as an endosymbiont in root nodules. Here, we use random barcode transposon sequencing (RB-TnSeq) to assay gene contributions of R. leguminosarum during competitive growth in the rhizosphere and colonisation of various plant species. This facilitated the identification of 189 genes commonly required for growth in diverse plant rhizospheres, mutation of 111 of which also affected subsequent root colonisation (rhizosphere progressive), and a further 119 genes necessary for colonisation. Common determinants reveal a need to synthesise essential compounds (amino acids, ribonucleotides, and cofactors), adapt metabolic function, respond to external stimuli, and withstand various stresses (such as changes in osmolarity). Additionally, chemotaxis and flagella-mediated motility are prerequisites for root colonisation. Many genes showed plant-specific dependencies highlighting significant adaptation to different plant species. This work provides a greater understanding of factors promoting rhizosphere fitness and root colonisation in plant-beneficial bacteria, facilitating their exploitation for agricultural benefit.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"6 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2024-04-26","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140817588","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}
Understanding the link between microbial community stability and assembly processes is crucial in microbial ecology. Here, we investigated whether the impact of biotic disturbances would depend on the processes controlling community assembly. For that, we performed an experiment using soil microcosms in which microbial communities assembled through different processes were invaded by Escherichia coli. We show that the ecological assembly process of the resident community plays a significant role in invader-resident competition, invader survival, and compositional stability of the resident community. Specifically, the resident communities primarily assembled through stochastic processes were more susceptible to invader survival. Besides, E. coli invasion acts as a biotic selection pressure, leading to competition between the invader and resident taxa, suppressing the stochasticity in the resident community. Taken together, this study provides empirical evidence for the interpretation of microbial community assemblage on their (potential) ecosystem functions and services, such as the prevention of pathogen establishment and the pathogenic states of soil microbiomes.
{"title":"Bridging ecological assembly process and community stability upon bacterial invasions","authors":"Xipeng Liu, Joana Falcão Salles","doi":"10.1093/ismejo/wrae066","DOIUrl":"https://doi.org/10.1093/ismejo/wrae066","url":null,"abstract":"Understanding the link between microbial community stability and assembly processes is crucial in microbial ecology. Here, we investigated whether the impact of biotic disturbances would depend on the processes controlling community assembly. For that, we performed an experiment using soil microcosms in which microbial communities assembled through different processes were invaded by Escherichia coli. We show that the ecological assembly process of the resident community plays a significant role in invader-resident competition, invader survival, and compositional stability of the resident community. Specifically, the resident communities primarily assembled through stochastic processes were more susceptible to invader survival. Besides, E. coli invasion acts as a biotic selection pressure, leading to competition between the invader and resident taxa, suppressing the stochasticity in the resident community. Taken together, this study provides empirical evidence for the interpretation of microbial community assemblage on their (potential) ecosystem functions and services, such as the prevention of pathogen establishment and the pathogenic states of soil microbiomes.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"2 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2024-04-25","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140648675","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}
Sarah Shah, Katherine E Dougan, Yibi Chen, Rosalyn Lo, Gemma Laird, Michael D A Fortuin, Subash K Rai, Valentine Murigneux, Anthony J Bellantuono, Mauricio Rodriguez-Lanetty, Debashish Bhattacharya, Cheong Xin Chan
Dinoflagellates in the family Symbiodiniaceae are taxonomically diverse, predominantly symbiotic lineages that are well-known for their association with corals. The ancestor of these taxa is believed to have been free-living. The establishment of symbiosis (i.e., symbiogenesis) is hypothesised to have occurred multiple times during Symbiodiniaceae evolution, but its impact on genome evolution of these taxa is largely unknown. Among Symbiodiniaceae, the genus Effrenium is a free-living lineage that is phylogenetically positioned between two robustly supported groups of genera within which symbiotic taxa have emerged. The apparent lack of symbiogenesis in Effrenium suggests that the ancestral features of Symbiodiniaceae may have been retained in this lineage. Here we present de novo assembled genomes (1.2–1.9 Gbp in size) and transcriptome data from three isolates of Effrenium voratum and conduct a comparative analysis that includes 16 Symbiodiniaceae taxa and the other dinoflagellates. Surprisingly, we find that genome reduction, which is often associated with a symbiotic lifestyle, predates the origin of Symbiodiniaceae. The free-living lifestyle distinguishes Effrenium from symbiotic Symbiodiniaceae vis-à-vis their longer introns, more-extensive mRNA editing, fewer (~30%) lineage-specific gene sets, and lower (~10%) level of pseudogenisation. These results demonstrate how genome reduction and the adaptation to distinct lifestyles intersect to drive diversification and genome evolution of Symbiodiniaceae.
{"title":"Massive genome reduction predates the divergence of Symbiodiniaceae dinoflagellates","authors":"Sarah Shah, Katherine E Dougan, Yibi Chen, Rosalyn Lo, Gemma Laird, Michael D A Fortuin, Subash K Rai, Valentine Murigneux, Anthony J Bellantuono, Mauricio Rodriguez-Lanetty, Debashish Bhattacharya, Cheong Xin Chan","doi":"10.1093/ismejo/wrae059","DOIUrl":"https://doi.org/10.1093/ismejo/wrae059","url":null,"abstract":"Dinoflagellates in the family Symbiodiniaceae are taxonomically diverse, predominantly symbiotic lineages that are well-known for their association with corals. The ancestor of these taxa is believed to have been free-living. The establishment of symbiosis (i.e., symbiogenesis) is hypothesised to have occurred multiple times during Symbiodiniaceae evolution, but its impact on genome evolution of these taxa is largely unknown. Among Symbiodiniaceae, the genus Effrenium is a free-living lineage that is phylogenetically positioned between two robustly supported groups of genera within which symbiotic taxa have emerged. The apparent lack of symbiogenesis in Effrenium suggests that the ancestral features of Symbiodiniaceae may have been retained in this lineage. Here we present de novo assembled genomes (1.2–1.9 Gbp in size) and transcriptome data from three isolates of Effrenium voratum and conduct a comparative analysis that includes 16 Symbiodiniaceae taxa and the other dinoflagellates. Surprisingly, we find that genome reduction, which is often associated with a symbiotic lifestyle, predates the origin of Symbiodiniaceae. The free-living lifestyle distinguishes Effrenium from symbiotic Symbiodiniaceae vis-à-vis their longer introns, more-extensive mRNA editing, fewer (~30%) lineage-specific gene sets, and lower (~10%) level of pseudogenisation. These results demonstrate how genome reduction and the adaptation to distinct lifestyles intersect to drive diversification and genome evolution of Symbiodiniaceae.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"82 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2024-04-24","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140642499","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}
Bettina Glasl, Heidi M Luter, Katarina Damjanovic, Katharina Kitzinger, Anna J Mueller, Leonie Mahler, Joan Pamela Engelberts, Laura Rix, Jay T Osvatic, Bela Hausmann, Joana Séneca, Holger Daims, Petra Pjevac, Michael Wagner
Ammonia-oxidising archaea and nitrite-oxidising bacteria are common members of marine sponge microbiomes. They derive energy for carbon fixation and growth from nitrification - the aerobic oxidation of ammonia to nitrite and further to nitrate - and are proposed to play essential roles in the carbon and nitrogen cycling of sponge holobionts. In this study, we characterise two novel nitrifying symbiont lineages, Candidatus Nitrosokoinonia and Candidatus Nitrosymbion in the marine sponge Coscinoderma matthewsi using a combination of molecular tools, in situ visualisation, and physiological rate measurements. Both represent a new genus in the ammonia-oxidising archaeal class Nitrososphaeria and the nitrite-oxidising bacterial order Nitrospirales, respectively. Furthermore, we show that larvae of this viviparous sponge are densely colonised by representatives of Ca. Nitrosokoinonia and Ca. Nitrosymbion indicating vertical transmission. In adults, the representatives of both symbiont genera are located extracellularly in the mesohyl. Comparative metagenome analyses and physiological data suggest that ammonia-oxidising archaeal symbionts of the genus Ca. Nitrosokoinonia strongly rely on endogenously produced nitrogenous compounds (i.e., ammonium, urea, nitriles/cyanides, and creatinine) rather than on exogenous ammonium sources taken up by the sponge. Additionally, the nitrite-oxidising bacterial symbionts of the genus Ca. Nitrosymbion may reciprocally support the ammonia-oxidisers with ammonia via the utilisation of sponge-derived urea and cyanate. Comparative analyses of published environmental 16S rRNA gene amplicon data revealed that Ca. Nitrosokoinonia and Ca. Nitrosymbion are widely distributed and predominantly associated with marine sponges and corals, suggesting a broad relevance of our findings.
{"title":"Co-occurring nitrifying symbiont lineages are vertically inherited and widespread in marine sponges","authors":"Bettina Glasl, Heidi M Luter, Katarina Damjanovic, Katharina Kitzinger, Anna J Mueller, Leonie Mahler, Joan Pamela Engelberts, Laura Rix, Jay T Osvatic, Bela Hausmann, Joana Séneca, Holger Daims, Petra Pjevac, Michael Wagner","doi":"10.1093/ismejo/wrae069","DOIUrl":"https://doi.org/10.1093/ismejo/wrae069","url":null,"abstract":"Ammonia-oxidising archaea and nitrite-oxidising bacteria are common members of marine sponge microbiomes. They derive energy for carbon fixation and growth from nitrification - the aerobic oxidation of ammonia to nitrite and further to nitrate - and are proposed to play essential roles in the carbon and nitrogen cycling of sponge holobionts. In this study, we characterise two novel nitrifying symbiont lineages, Candidatus Nitrosokoinonia and Candidatus Nitrosymbion in the marine sponge Coscinoderma matthewsi using a combination of molecular tools, in situ visualisation, and physiological rate measurements. Both represent a new genus in the ammonia-oxidising archaeal class Nitrososphaeria and the nitrite-oxidising bacterial order Nitrospirales, respectively. Furthermore, we show that larvae of this viviparous sponge are densely colonised by representatives of Ca. Nitrosokoinonia and Ca. Nitrosymbion indicating vertical transmission. In adults, the representatives of both symbiont genera are located extracellularly in the mesohyl. Comparative metagenome analyses and physiological data suggest that ammonia-oxidising archaeal symbionts of the genus Ca. Nitrosokoinonia strongly rely on endogenously produced nitrogenous compounds (i.e., ammonium, urea, nitriles/cyanides, and creatinine) rather than on exogenous ammonium sources taken up by the sponge. Additionally, the nitrite-oxidising bacterial symbionts of the genus Ca. Nitrosymbion may reciprocally support the ammonia-oxidisers with ammonia via the utilisation of sponge-derived urea and cyanate. Comparative analyses of published environmental 16S rRNA gene amplicon data revealed that Ca. Nitrosokoinonia and Ca. Nitrosymbion are widely distributed and predominantly associated with marine sponges and corals, suggesting a broad relevance of our findings.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"18 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2024-04-23","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140651348","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}
Zoila I Alvarez-Aponte, Alekhya M Govindaraju, Zachary F Hallberg, Alexa M Nicolas, Myka A Green, Kenny C Mok, Citlali Fonseca-Garcia, Devin Coleman-Derr, Eoin L Brodie, Hans K Carlson, Michiko E Taga
Soil microbial communities impact carbon sequestration and release, biogeochemical cycling, and agricultural yields. These global effects rely on metabolic interactions that modulate community composition and function. However, the physicochemical and taxonomic complexity of soil and the scarcity of available isolates for phenotypic testing are significant barriers to studying soil microbial interactions. Corrinoids—the vitamin B12 family of cofactors—are critical for microbial metabolism, yet they are synthesized by only a subset of microbiome members. Here, we evaluated corrinoid production and dependence in soil bacteria as a model to investigate the ecological roles of microorganisms involved in metabolic interactions. We isolated and characterized a taxonomically diverse collection of 161 soil bacteria from a single study site. Most corrinoid-dependent bacteria in the collection prefer B12 over other corrinoids, while all tested producers synthesize B12, indicating metabolic compatibility between producers and dependents in the collection. Furthermore, a subset of producers release B12 at levels sufficient to support dependent isolates in laboratory culture at estimated ratios of up to 1000 dependents per producer. Within our isolate collection, we did not find strong phylogenetic patterns in corrinoid production or dependence. Upon investigating trends in the phylogenetic dispersion of corrinoid metabolism categories across sequenced bacteria from various environments, we found that these traits are conserved in 47 out of 85 genera. Together, these phenotypic and genomic results provide evidence for corrinoid-based metabolic interactions among bacteria and provide a framework for the study of nutrient-sharing ecological interactions in microbial communities.
{"title":"Phylogenetic distribution and experimental characterization of corrinoid production and dependence in soil bacterial isolates","authors":"Zoila I Alvarez-Aponte, Alekhya M Govindaraju, Zachary F Hallberg, Alexa M Nicolas, Myka A Green, Kenny C Mok, Citlali Fonseca-Garcia, Devin Coleman-Derr, Eoin L Brodie, Hans K Carlson, Michiko E Taga","doi":"10.1093/ismejo/wrae068","DOIUrl":"https://doi.org/10.1093/ismejo/wrae068","url":null,"abstract":"Soil microbial communities impact carbon sequestration and release, biogeochemical cycling, and agricultural yields. These global effects rely on metabolic interactions that modulate community composition and function. However, the physicochemical and taxonomic complexity of soil and the scarcity of available isolates for phenotypic testing are significant barriers to studying soil microbial interactions. Corrinoids—the vitamin B12 family of cofactors—are critical for microbial metabolism, yet they are synthesized by only a subset of microbiome members. Here, we evaluated corrinoid production and dependence in soil bacteria as a model to investigate the ecological roles of microorganisms involved in metabolic interactions. We isolated and characterized a taxonomically diverse collection of 161 soil bacteria from a single study site. Most corrinoid-dependent bacteria in the collection prefer B12 over other corrinoids, while all tested producers synthesize B12, indicating metabolic compatibility between producers and dependents in the collection. Furthermore, a subset of producers release B12 at levels sufficient to support dependent isolates in laboratory culture at estimated ratios of up to 1000 dependents per producer. Within our isolate collection, we did not find strong phylogenetic patterns in corrinoid production or dependence. Upon investigating trends in the phylogenetic dispersion of corrinoid metabolism categories across sequenced bacteria from various environments, we found that these traits are conserved in 47 out of 85 genera. Together, these phenotypic and genomic results provide evidence for corrinoid-based metabolic interactions among bacteria and provide a framework for the study of nutrient-sharing ecological interactions in microbial communities.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"233 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2024-04-22","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140637614","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}
Dilem Ruhluel, Lewis Fisher, Thomas E Barton, Hollie Leighton, Sumit Kumar, Paula Amores Morillo, Siobhan O’Brien, Joanne L Fothergill, Daniel R Neill
Pseudomonas aeruginosa is a cause of chronic respiratory tract infections in people with cystic fibrosis (CF), non-CF bronchiectasis and chronic obstructive pulmonary disease. Prolonged infection allows accumulation of mutations and horizontal gene transfer, increasing the likelihood of adaptive phenotypic traits. Adaptation is proposed to arise first in bacterial populations colonising upper airway environments. Here, we model this process using an experimental evolution approach. P. aeruginosa PAO1, which is not airway adapted, was serially passaged, separately, in media chemically reflective of upper or lower airway environments. To explore whether the CF environment selects for unique traits, we separately passaged PAO1 in airway-mimicking media with or without CF-specific factors. Our findings demonstrated that all airway environments – sinus and lungs, under CF and non-CF conditions – selected for loss of twitching motility, increased resistance to multiple antibiotic classes and a hyper-biofilm phenotype. These traits conferred increased airway colonisation potential in an in vivo model. CF-like conditions exerted stronger selective pressures, leading to emergence of more pronounced phenotypes. Loss of twitching was associated with mutations in type IV pili genes. Type IV pili mediate surface attachment, twitching and induction of cAMP signalling. We additionally identified multiple evolutionary routes to increased biofilm formation involving regulation of cyclic-di-GMP signalling. These included loss of function mutations in bifA and dipA phosphodiesterase genes and activating mutations in the siaA phosphatase. These data highlight that airway environments select for traits associated with sessile lifestyles and suggest upper airway niches support emergence of phenotypes that promote establishment of lung infection.
{"title":"Secondary messenger signalling influences Pseudomonas aeruginosa adaptation to sinus and lung environments","authors":"Dilem Ruhluel, Lewis Fisher, Thomas E Barton, Hollie Leighton, Sumit Kumar, Paula Amores Morillo, Siobhan O’Brien, Joanne L Fothergill, Daniel R Neill","doi":"10.1093/ismejo/wrae065","DOIUrl":"https://doi.org/10.1093/ismejo/wrae065","url":null,"abstract":"Pseudomonas aeruginosa is a cause of chronic respiratory tract infections in people with cystic fibrosis (CF), non-CF bronchiectasis and chronic obstructive pulmonary disease. Prolonged infection allows accumulation of mutations and horizontal gene transfer, increasing the likelihood of adaptive phenotypic traits. Adaptation is proposed to arise first in bacterial populations colonising upper airway environments. Here, we model this process using an experimental evolution approach. P. aeruginosa PAO1, which is not airway adapted, was serially passaged, separately, in media chemically reflective of upper or lower airway environments. To explore whether the CF environment selects for unique traits, we separately passaged PAO1 in airway-mimicking media with or without CF-specific factors. Our findings demonstrated that all airway environments – sinus and lungs, under CF and non-CF conditions – selected for loss of twitching motility, increased resistance to multiple antibiotic classes and a hyper-biofilm phenotype. These traits conferred increased airway colonisation potential in an in vivo model. CF-like conditions exerted stronger selective pressures, leading to emergence of more pronounced phenotypes. Loss of twitching was associated with mutations in type IV pili genes. Type IV pili mediate surface attachment, twitching and induction of cAMP signalling. We additionally identified multiple evolutionary routes to increased biofilm formation involving regulation of cyclic-di-GMP signalling. These included loss of function mutations in bifA and dipA phosphodiesterase genes and activating mutations in the siaA phosphatase. These data highlight that airway environments select for traits associated with sessile lifestyles and suggest upper airway niches support emergence of phenotypes that promote establishment of lung infection.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"1 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2024-04-22","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140637610","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}
Josep Ramoneda, Kunkun Fan, Jane M Lucas, Haiyan Chu, Andrew Bissett, Michael S Strickland, Noah Fierer
Flagellar motility is a key bacterial trait as it allows bacteria to navigate their immediate surroundings. Not all bacteria are capable of flagellar motility, and the distribution of this trait, its ecological associations, and the life history strategies of flagellated taxa remain poorly characterized. We developed and validated a genome-based approach to infer the potential for flagellar motility across 12 bacterial phyla (26 192 genomes in total). The capacity for flagellar motility was associated with a higher prevalence of genes for carbohydrate metabolism and higher maximum potential growth rates, suggesting that flagellar motility is more prevalent in environments with higher carbon availability. To test this hypothesis, we applied a method to infer the prevalence of flagellar motility in whole bacterial communities from metagenomic data, and quantified the prevalence of flagellar motility across 4 independent field studies that each captured putative gradients in soil carbon availability (148 metagenomes). As expected, we observed a positive relationship between the prevalence of bacterial flagellar motility and soil carbon availability in all datasets. Since soil carbon availability is often correlated with other factors that could influence the prevalence of flagellar motility, we validated these observations using metagenomic data acquired from a soil incubation experiment where carbon availability was directly manipulated with glucose amendments. This confirmed that the prevalence of bacterial flagellar motility is consistently associated with soil carbon availability over other potential confounding factors. This work highlights the value of combining predictive genomic and metagenomic approaches to expand our understanding of microbial phenotypic traits and reveal their general environmental associations.
{"title":"Ecological relevance of flagellar motility in soil bacterial communities","authors":"Josep Ramoneda, Kunkun Fan, Jane M Lucas, Haiyan Chu, Andrew Bissett, Michael S Strickland, Noah Fierer","doi":"10.1093/ismejo/wrae067","DOIUrl":"https://doi.org/10.1093/ismejo/wrae067","url":null,"abstract":"Flagellar motility is a key bacterial trait as it allows bacteria to navigate their immediate surroundings. Not all bacteria are capable of flagellar motility, and the distribution of this trait, its ecological associations, and the life history strategies of flagellated taxa remain poorly characterized. We developed and validated a genome-based approach to infer the potential for flagellar motility across 12 bacterial phyla (26 192 genomes in total). The capacity for flagellar motility was associated with a higher prevalence of genes for carbohydrate metabolism and higher maximum potential growth rates, suggesting that flagellar motility is more prevalent in environments with higher carbon availability. To test this hypothesis, we applied a method to infer the prevalence of flagellar motility in whole bacterial communities from metagenomic data, and quantified the prevalence of flagellar motility across 4 independent field studies that each captured putative gradients in soil carbon availability (148 metagenomes). As expected, we observed a positive relationship between the prevalence of bacterial flagellar motility and soil carbon availability in all datasets. Since soil carbon availability is often correlated with other factors that could influence the prevalence of flagellar motility, we validated these observations using metagenomic data acquired from a soil incubation experiment where carbon availability was directly manipulated with glucose amendments. This confirmed that the prevalence of bacterial flagellar motility is consistently associated with soil carbon availability over other potential confounding factors. This work highlights the value of combining predictive genomic and metagenomic approaches to expand our understanding of microbial phenotypic traits and reveal their general environmental associations.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"19 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2024-04-22","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140637707","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}
Many organisms have formed symbiotic relationships with nitrogen (N)-fixing bacteria to overcome N limitation. Diatoms in the family Rhopalodiaceae host unicellular, N-fixing cyanobacterial endosymbionts called spheroid bodies (SBs). Although this relationship is relatively young, SBs share many key features with older endosymbionts, including coordinated cell division and genome reduction. Unlike free-living relatives that fix N exclusively at night, SBs fix N largely during the day; however, how SB metabolism is regulated and coordinated with the host is not yet understood. We compared four SB genomes, including those from two new host species (Rhopalodia gibba and Epithemia adnata), to build a genome-wide phylogeny which provides a better understanding of SB evolutionary origins. Contrary to models of endosymbiotic genome reduction, the SB chromosome is unusually stable for an endosymbiont genome, likely due to the early loss of all mobile elements. Transcriptomic data for the R. gibba SB and host organelles addressed whether and how the allocation of transcriptional resources depends on light and nitrogen availability. Whereas allocation to the SB was high under all conditions, relative expression of chloroplast photosynthesis genes increased in the absence of nitrate, but this pattern was suppressed by nitrate addition. SB expression of catabolism genes was generally greater during daytime rather than at night, although the magnitude of diurnal changes in expression was modest compared to free-living cyanobacteria. We conclude that SB daytime catabolism likely supports N-fixation by linking the process to host photosynthetic carbon fixation.
{"title":"Diurnal transcriptional variation is reduced in a nitrogen-fixing diatom endosymbiont","authors":"Heidi Abresch, Tisza Bell, Scott R Miller","doi":"10.1093/ismejo/wrae064","DOIUrl":"https://doi.org/10.1093/ismejo/wrae064","url":null,"abstract":"Many organisms have formed symbiotic relationships with nitrogen (N)-fixing bacteria to overcome N limitation. Diatoms in the family Rhopalodiaceae host unicellular, N-fixing cyanobacterial endosymbionts called spheroid bodies (SBs). Although this relationship is relatively young, SBs share many key features with older endosymbionts, including coordinated cell division and genome reduction. Unlike free-living relatives that fix N exclusively at night, SBs fix N largely during the day; however, how SB metabolism is regulated and coordinated with the host is not yet understood. We compared four SB genomes, including those from two new host species (Rhopalodia gibba and Epithemia adnata), to build a genome-wide phylogeny which provides a better understanding of SB evolutionary origins. Contrary to models of endosymbiotic genome reduction, the SB chromosome is unusually stable for an endosymbiont genome, likely due to the early loss of all mobile elements. Transcriptomic data for the R. gibba SB and host organelles addressed whether and how the allocation of transcriptional resources depends on light and nitrogen availability. Whereas allocation to the SB was high under all conditions, relative expression of chloroplast photosynthesis genes increased in the absence of nitrate, but this pattern was suppressed by nitrate addition. SB expression of catabolism genes was generally greater during daytime rather than at night, although the magnitude of diurnal changes in expression was modest compared to free-living cyanobacteria. We conclude that SB daytime catabolism likely supports N-fixation by linking the process to host photosynthetic carbon fixation.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"46 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2024-04-18","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140620064","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}
Connecting genes to phenotypic traits in bacteria is often challenging because of a lack of environmental context in laboratory settings. Laboratory-based model ecosystems offer a means to better account for environmental conditions compared to standard planktonic cultures, and can help link genotypes and phenotypes. Here, we present a simple, cost-effective, laboratory-based model ecosystem to study aerobic methane-oxidizing bacteria (methanotrophs) within the methane-oxygen counter gradient typically found in the natural environment of these organisms. Culturing the methanotroph Methylomonas sp. strain LW13 in this system resulted in formation of a distinct horizontal band at the intersection of the counter gradient, which we discovered was not due to increased numbers of bacteria at this location but instead to an increased amount of polysaccharides. We also discovered that different methanotrophic taxa form polysaccharide bands with distinct locations and morphologies when grown in the methane-oxygen counter gradient. By comparing transcriptomic data from LW13 growing within and surrounding this band, we identified genes upregulated within the band and validated their involvement in growth and band formation within the model ecosystem using knockout strains. Notably, deletion of these genes did not negatively affect growth using standard planktonic culturing methods. This work highlights the use of a laboratory-based model ecosystem that more closely mimics the natural environment to uncover bacterial phenotypes missing from standard laboratory conditions, and to link these phenotypes with their genetic determinants.
{"title":"Linking methanotroph phenotypes to genotypes using a simple spatially resolved model ecosystem","authors":"Delaney G Beals, Aaron W Puri","doi":"10.1093/ismejo/wrae060","DOIUrl":"https://doi.org/10.1093/ismejo/wrae060","url":null,"abstract":"Connecting genes to phenotypic traits in bacteria is often challenging because of a lack of environmental context in laboratory settings. Laboratory-based model ecosystems offer a means to better account for environmental conditions compared to standard planktonic cultures, and can help link genotypes and phenotypes. Here, we present a simple, cost-effective, laboratory-based model ecosystem to study aerobic methane-oxidizing bacteria (methanotrophs) within the methane-oxygen counter gradient typically found in the natural environment of these organisms. Culturing the methanotroph Methylomonas sp. strain LW13 in this system resulted in formation of a distinct horizontal band at the intersection of the counter gradient, which we discovered was not due to increased numbers of bacteria at this location but instead to an increased amount of polysaccharides. We also discovered that different methanotrophic taxa form polysaccharide bands with distinct locations and morphologies when grown in the methane-oxygen counter gradient. By comparing transcriptomic data from LW13 growing within and surrounding this band, we identified genes upregulated within the band and validated their involvement in growth and band formation within the model ecosystem using knockout strains. Notably, deletion of these genes did not negatively affect growth using standard planktonic culturing methods. This work highlights the use of a laboratory-based model ecosystem that more closely mimics the natural environment to uncover bacterial phenotypes missing from standard laboratory conditions, and to link these phenotypes with their genetic determinants.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"443 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2024-04-16","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140603663","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}
Lauren E Manck, Tyler H Coale, Brandon M Stephens, Kiefer O Forsch, Lihini I Aluwihare, Christopher L Dupont, Andrew E Allen, Katherine A Barbeau
Iron is an essential nutrient for all microorganisms in the marine environment. Iron limitation of primary production has been well documented across a significant portion of the global surface ocean, but much less is known regarding the potential for iron limitation of the marine heterotrophic microbial community. In this work, we characterize the transcriptomic response of the heterotrophic bacterial community to iron additions in the California Current System, an eastern boundary upwelling system, to detect in situ iron stress of heterotrophic bacteria. Changes in gene expression in response to iron availability by heterotrophic bacteria were detected under conditions of high productivity when carbon limitation was relieved but when iron availability remained low. The ratio of particulate organic carbon to dissolved iron emerged as a biogeochemical proxy for iron limitation of heterotrophic bacteria in this system. Iron stress was characterized by high expression levels of iron transport pathways and decreased expression of iron-containing enzymes involved in carbon metabolism, where a majority of the heterotrophic bacterial iron requirement resides. Expression of iron stress biomarkers, as identified in the iron-addition experiments, was also detected in situ. These results suggest iron availability will impact the processing of organic matter by heterotrophic bacteria with potential consequences for the marine biological carbon pump.
{"title":"Iron limitation of heterotrophic bacteria in the California current system tracks relative availability of organic carbon and iron","authors":"Lauren E Manck, Tyler H Coale, Brandon M Stephens, Kiefer O Forsch, Lihini I Aluwihare, Christopher L Dupont, Andrew E Allen, Katherine A Barbeau","doi":"10.1093/ismejo/wrae061","DOIUrl":"https://doi.org/10.1093/ismejo/wrae061","url":null,"abstract":"Iron is an essential nutrient for all microorganisms in the marine environment. Iron limitation of primary production has been well documented across a significant portion of the global surface ocean, but much less is known regarding the potential for iron limitation of the marine heterotrophic microbial community. In this work, we characterize the transcriptomic response of the heterotrophic bacterial community to iron additions in the California Current System, an eastern boundary upwelling system, to detect in situ iron stress of heterotrophic bacteria. Changes in gene expression in response to iron availability by heterotrophic bacteria were detected under conditions of high productivity when carbon limitation was relieved but when iron availability remained low. The ratio of particulate organic carbon to dissolved iron emerged as a biogeochemical proxy for iron limitation of heterotrophic bacteria in this system. Iron stress was characterized by high expression levels of iron transport pathways and decreased expression of iron-containing enzymes involved in carbon metabolism, where a majority of the heterotrophic bacterial iron requirement resides. Expression of iron stress biomarkers, as identified in the iron-addition experiments, was also detected in situ. These results suggest iron availability will impact the processing of organic matter by heterotrophic bacteria with potential consequences for the marine biological carbon pump.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"74 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2024-04-16","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140603920","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}
京公网安备 11010802042870号
京ICP备2023020795号-1
扫码关注我们
求助内容：
应助结果提醒方式：