The ISME JournalPub Date : 2024-01-29DOI: 10.1093/ismejo/wrae018
Samuel M McNichol, Fernando Sanchez-Quete, Stephanie K Loeb, Andreas Teske, Sunita R Shah Walter, Nagissa Mahmoudi
{"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}
The ISME JournalPub Date : 2024-01-28DOI: 10.1093/ismejo/wrae014
Álvaro Morón, Alaa E Tarhouchi, Iván Belinchón, Juan M Valenzuela, Patricia de Francisco, Ana Martín-González, Francisco Amaro
{"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}
{"title":"VapC10 toxin of the legume symbiont Sinorhizobium meliloti targets tRNASer and controls intracellular lifestyle","authors":"Camille Syska, Aurélie Kiers, Corinne Rancurel, Marc Bailly-Bechet, Justine Lipuma, Geneviève Alloing, Isabelle Garcia, Laurence Dupont","doi":"10.1093/ismejo/wrae015","DOIUrl":"https://doi.org/10.1093/ismejo/wrae015","url":null,"abstract":"The soil bacterium Sinorhizobium meliloti can establish a nitrogen fixing symbiosis with the model legume Medicago truncatula. The rhizobia induce the formation of a specialized root organ called nodule, where they differentiate into bacteroids and reduce atmospheric nitrogen into ammonia. Little is known on the mechanisms involved in nodule senescence onset and in bacteroid survival inside the infected plant cells. Whereas Toxin-Antitoxin (TA) systems have been shown to promote intracellular survival within host cells in human pathogenic bacteria, their role in symbiotic bacteria was rarely investigated. S. meliloti encodes several TA systems, mainly of the VapBC family. Here we present the functional characterization, through a multidisciplinary approach, of the VapBC10 TA system of S. meliloti. Following a MORE RNA-seq analysis, we demonstrated that the VapC10 toxin is an RNase that cleaves the anticodon loop of two tRNASer. Thereafter, a bioinformatics approach was used to predict VapC10 targets in bacteroids. This analysis suggests that toxin activation triggers a specific proteome reprogramming that could limit nitrogen fixation capability and viability of bacteroids. Accordingly, a vapC10 mutant induces a delayed senescence in nodules, associated to an enhanced bacteroid survival. VapBC10 TA system could contribute to S. meliloti adaptation to symbiotic lifestyle, in response to plant nitrogen status.","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":"139577528","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 ISME JournalPub Date : 2024-01-28DOI: 10.1093/ismejo/wrae001
Tess F Hutchinson, Adam J Kessler, Wei Wen Wong, Puspitaningsih Hall, Pok Man Leung, Thanavit Jirapanjawat, Chris Greening, Ronnie N Glud, Perran L M Cook
{"title":"Microorganisms oxidize glucose through distinct pathways in permeable and cohesive sediments","authors":"Tess F Hutchinson, Adam J Kessler, Wei Wen Wong, Puspitaningsih Hall, Pok Man Leung, Thanavit Jirapanjawat, Chris Greening, Ronnie N Glud, Perran L M Cook","doi":"10.1093/ismejo/wrae001","DOIUrl":"https://doi.org/10.1093/ismejo/wrae001","url":null,"abstract":"In marine sediments, microbial degradation of organic matter under anoxic conditions is generally thought to proceed through fermentation to volatile fatty acids (VFA), which are then oxidized to CO2 coupled to the reduction of terminal electron acceptors (e.g. nitrate, iron, manganese and sulfate). It has been suggested that, in environments with a highly variable oxygen regime, fermentation mediated by facultative anaerobic bacteria (uncoupled to external terminal electron acceptors) becomes the dominant process. Here, we present the first direct evidence for this fermentation using a novel differentially-labelled glucose isotopologue assay that distinguishes between CO2 produced from respiration and fermentation. Using this approach, we measured the relative contribution of respiration and fermentation of glucose in a range of permeable (sandy) and cohesive (muddy) sediments, as well as four bacterial isolates. Under anoxia, microbial communities adapted to high energy sandy or bioturbated sites mediate fermentation via the Embden-Meyerhof-Parnas (EMP) pathway, in a manner uncoupled from anaerobic respiration. Prolonged anoxic incubation suggests this uncoupling lasts up to 160 hours. In contrast, microbial communities in anoxic muddy sediments (smaller median grain size) generally completely oxidized 13C glucose to 13CO2, consistent with the classical redox cascade model. We also unexpectedly observed that fermentation occurred under oxic conditions in permeable sediments. These observations were further confirmed using pure cultures of four bacteria isolated from permeable sediments. Our results suggest microbial communities adapted to variable oxygen regimes metabolise glucose (and likely other organic molecules) through fermentation uncoupled to respiration during transient anoxic conditions.","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":"139577391","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 ISME JournalPub Date : 2024-01-24DOI: 10.1093/ismejo/wrae008
Diana P Baquero, Eduardo A Bignon, Mart Krupovic
{"title":"Pleomorphic viruses establish stable relationship with marine hyperthermophilic archaea","authors":"Diana P Baquero, Eduardo A Bignon, Mart Krupovic","doi":"10.1093/ismejo/wrae008","DOIUrl":"https://doi.org/10.1093/ismejo/wrae008","url":null,"abstract":"Non-lytic viruses with enveloped pleomorphic virions (family Pleolipoviridae) are ubiquitous in hypersaline environments across the globe and are associated with nearly all major lineages of halophilic archaea. However, their existence in other ecosystems remains largely unknown. Here, we show that evolutionarily related viruses also infect hyperthermophilic archaea thriving in deep-sea hydrothermal vents. Archaeoglobus veneficus pleomorphic virus 1 (AvPV1), the first virus described for any member of the class Archaeoglobi, encodes a morphogenetic module typical of pleolipoviruses, including the characteristic VP4-like membrane fusion protein. We show that AvPV1 is a non-lytic virus chronically produced in liquid cultures without substantially affecting the growth dynamics of its host with a stable virus-to-host ratio of ~1. Mining of genomic and metagenomic databases revealed broad distribution of AvPV1-like viruses in geographically remote hydrothermal vents. Comparative genomics, coupled with phylogenetic analysis of VP4-like fusogens revealed deep divergence of pleomorphic viruses infecting halophilic, methanogenic, and hyperthermophilic archaea, signifying niche separation and coevolution of the corresponding virus-host pairs. Hence, we propose a new virus family, “Thalassapleoviridae”, for classification of the marine hyperthermophilic virus AvPV1 and its relatives. Collectively, our results provide insights into the diversity and evolution of pleomorphic viruses beyond hypersaline environments.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":null,"pages":null},"PeriodicalIF":0.0,"publicationDate":"2024-01-24","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"139568357","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 ISME JournalPub Date : 2024-01-24DOI: 10.1093/ismejo/wrae006
Hong-Bin Liu, Hong-Xia Sun, Li-Qiong Du, Ling-Li Jiang, Lin-An Zhang, Yin-Yao Qi, Jun Cai, Feng Yu
{"title":"Rice receptor kinase FLR7 regulates rhizosphere oxygen levels and enriches the dominant Anaeromyxobacter that improves submergence tolerance in rice","authors":"Hong-Bin Liu, Hong-Xia Sun, Li-Qiong Du, Ling-Li Jiang, Lin-An Zhang, Yin-Yao Qi, Jun Cai, Feng Yu","doi":"10.1093/ismejo/wrae006","DOIUrl":"https://doi.org/10.1093/ismejo/wrae006","url":null,"abstract":"Oxygen is one of the determinants of root microbiome formation. However, whether plants regulate rhizosphere oxygen levels to affect microbiota composition and the underlying molecular mechanisms remain elusive. The receptor-like kinase (RLK) family member FERONIA modulates the growth–defense tradeoff in Arabidopsis. Here, we established that rice FERONIA-like RLK 7 (FLR7) controls rhizosphere oxygen levels by methylene blue staining, oxygen flux and potential measurements. The formation of oxygen-transporting aerenchyma in roots is negatively regulated by FLR7. We further characterized the root microbiota of 11 FLR mutants including flr7 and wild-type Nipponbare (Nip) grown in the field by 16S ribosomal RNA gene profiling and demonstrated that the 11 FLRs are involved in regulating rice root microbiome formation. The most abundant anaerobic-dependent genus Anaeromyxobacter in the Nip root microbiota was less abundant in the root microbiota of all these mutants, and this contributed the most to the community differences between most mutants and Nip. Metagenomic sequencing revealed that flr7 increases aerobic respiration and decreases anaerobic respiration in the root microbiome. Finally, we showed that a representative Anaeromyxobacter strain improved submergence tolerance in rice via FLR7. Collectively, our findings indicate that FLR7 mediates changes in rhizosphere oxygen levels and enriches the beneficial dominant genus Anaeromyxobacter and may provide insights for developing plant flood prevention strategies via the use of environment-specific functional soil microorganisms.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":null,"pages":null},"PeriodicalIF":0.0,"publicationDate":"2024-01-24","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"139568355","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 ISME JournalPub Date : 2024-01-24DOI: 10.1093/ismejo/wrae010
Maria Caballol, Miguel Ángel Redondo, Núria Catalán, Tamara Corcobado, Thomas Jung, Benoît Marçais, Ivan Milenković, Miguel Nemesio-Gorriz, Jan Stenlid, Jonàs Oliva
{"title":"Climate acts as an environmental filter to plant pathogens","authors":"Maria Caballol, Miguel Ángel Redondo, Núria Catalán, Tamara Corcobado, Thomas Jung, Benoît Marçais, Ivan Milenković, Miguel Nemesio-Gorriz, Jan Stenlid, Jonàs Oliva","doi":"10.1093/ismejo/wrae010","DOIUrl":"https://doi.org/10.1093/ismejo/wrae010","url":null,"abstract":"Climate shapes the distribution of plant-associated microbes such as mycorrhizal and endophytic fungi. However, the role of climate in plant pathogen community assembly is less understood. Here, we explored the role of climate in the assembly of Phytophthora communities at >250 sites along a latitudinal gradient from Spain to northern Sweden and an altitudinal gradient from the Spanish Pyrenees to lowland areas. Communities were detected by ITS sequencing of river filtrates. Mediation analysis supported the role of climate in the biogeography of Phytophthora and ruled out other environmental factors such as geography or tree diversity. Comparisons of functional and species diversity showed that environmental filtering dominated over competitive exclusion in Europe. Temperature and precipitation acted as environmental filters at different extremes of the gradients. In northern regions, winter temperatures acted as an environmental filter on Phytophthora community assembly, selecting species adapted to survive low minimum temperatures. In southern latitudes, a hot dry climate was the main environmental filter, resulting in communities dominated by drought-tolerant Phytophthora species with thick oospore walls, a high optimum temperature for growth and a high maximum temperature limit for growth. By taking a community ecology approach, we show that the establishment of Phytophthora plant pathogens in Europe is mainly restricted by cold temperatures.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":null,"pages":null},"PeriodicalIF":0.0,"publicationDate":"2024-01-24","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"139568356","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 ISME JournalPub Date : 2024-01-24DOI: 10.1093/ismejo/wrae011
Nobuto Takeuchi, Matthew S Fullmer, Danielle J Maddock, Anthony M Poole
{"title":"The constructive black queen hypothesis: new functions can evolve under conditions favouring gene loss","authors":"Nobuto Takeuchi, Matthew S Fullmer, Danielle J Maddock, Anthony M Poole","doi":"10.1093/ismejo/wrae011","DOIUrl":"https://doi.org/10.1093/ismejo/wrae011","url":null,"abstract":"Duplication is a major route for emergence of new gene functions. However, emergence of new gene function via this route may be reduced in prokaryotes, as redundant genes are often rapidly purged. In lineages with compact, streamlined genomes, it thus appears challenging for novel function to emerge via duplication and divergence. A further pressure contributing to gene loss occurs under Black Queen dynamics, as cheaters that lose the capacity to produce a public good can instead acquire it from neighbouring producers. We propose that Black Queen dynamics can favour the emergence of new function because under an emerging Black Queen dynamic there is high gene redundancy, spread across a community of interacting cells. Using computational modelling, we demonstrate that new gene functions can emerge under Black Queen dynamics. This result holds even if there is deletion bias due to low duplication rates and selection against redundant gene copies resulting from the high cost associated with carrying a locus. However, when the public good production costs are high, Black Queen dynamics impede fixation of new function. Our results expand the mechanisms by which new gene function can emerge in prokaryotic systems.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":null,"pages":null},"PeriodicalIF":0.0,"publicationDate":"2024-01-24","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"139568358","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}