ISME JournalPub Date : 2024-01-08DOI: 10.1093/ismejo/wrae054
Yi Han Tan, Patricio Arros, Camilo Berríos-Pastén, Indrik Wijaya, Wilson H W Chu, Yahua Chen, Guoxiang Cheam, Ahmad Nazri Mohamed Naim, Andrés E Marcoleta, Aarthi Ravikrishnan, Niranjan Nagarajan, Rosalba Lagos, Yunn-Hwen Gan
{"title":"Hypervirulent Klebsiella pneumoniae employs genomic island encoded toxins against bacterial competitors in the gut.","authors":"Yi Han Tan, Patricio Arros, Camilo Berríos-Pastén, Indrik Wijaya, Wilson H W Chu, Yahua Chen, Guoxiang Cheam, Ahmad Nazri Mohamed Naim, Andrés E Marcoleta, Aarthi Ravikrishnan, Niranjan Nagarajan, Rosalba Lagos, Yunn-Hwen Gan","doi":"10.1093/ismejo/wrae054","DOIUrl":"10.1093/ismejo/wrae054","url":null,"abstract":"<p><p>The hypervirulent lineages of Klebsiella pneumoniae (HvKp) cause invasive infections such as Klebsiella-liver abscess. Invasive infection often occurs after initial colonization of the host gastrointestinal tract by HvKp. Over 80% of HvKp isolates belong to the clonal group 23 sublineage I that has acquired genomic islands (GIs) GIE492 and ICEKp10. Our analysis of 12 361 K. pneumoniae genomes revealed that GIs GIE492 and ICEKp10 are co-associated with the CG23-I and CG10118 HvKp lineages. GIE492 and ICEKp10 enable HvKp to make a functional bacteriocin microcin E492 (mccE492) and the genotoxin colibactin, respectively. We discovered that GIE492 and ICEKp10 play cooperative roles and enhance gastrointestinal colonization by HvKp. Colibactin is the primary driver of this effect, modifying gut microbiome diversity. Our in vitro assays demonstrate that colibactin and mccE492 kill or inhibit a range of Gram-negative Klebsiella species and Escherichia coli strains, including Gram-positive bacteria, sometimes cooperatively. Moreover, mccE492 and colibactin kill human anaerobic gut commensals that are similar to the taxa found altered by colibactin in the mouse intestines. Our findings suggest that GIs GIE492 and ICEKp10 enable HvKp to kill several commensal bacterial taxa during interspecies interactions in the gut. Thus, acquisition of GIE492 and ICEKp10 could enable better carriage in host populations and explain the dominance of the CG23-I HvKp lineage.</p>","PeriodicalId":50271,"journal":{"name":"ISME Journal","volume":" ","pages":""},"PeriodicalIF":10.8,"publicationDate":"2024-01-08","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11020217/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140319832","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"环境科学与生态学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
ISME JournalPub Date : 2024-01-08DOI: 10.1093/ismejo/wrae091
Rachel C Beaver, Josh D Neufeld
{"title":"Microbial ecology of the deep terrestrial subsurface.","authors":"Rachel C Beaver, Josh D Neufeld","doi":"10.1093/ismejo/wrae091","DOIUrl":"10.1093/ismejo/wrae091","url":null,"abstract":"<p><p>The terrestrial subsurface hosts microbial communities that, collectively, are predicted to comprise as many microbial cells as global surface soils. Although initially thought to be associated with deposited organic matter, deep subsurface microbial communities are supported by chemolithoautotrophic primary production, with hydrogen serving as an important source of electrons. Despite recent progress, relatively little is known about the deep terrestrial subsurface compared to more commonly studied environments. Understanding the composition of deep terrestrial subsurface microbial communities and the factors that influence them is of importance because of human-associated activities including long-term storage of used nuclear fuel, carbon capture, and storage of hydrogen for use as an energy vector. In addition to identifying deep subsurface microorganisms, recent research focuses on identifying the roles of microorganisms in subsurface communities, as well as elucidating myriad interactions-syntrophic, episymbiotic, and viral-that occur among community members. In recent years, entirely new groups of microorganisms (i.e. candidate phyla radiation bacteria and Diapherotrites, Parvarchaeota, Aenigmarchaeota, Nanoloarchaeota, Nanoarchaeota archaea) have been discovered in deep terrestrial subsurface environments, suggesting that much remains unknown about this biosphere. This review explores the historical context for deep terrestrial subsurface microbial ecology and highlights recent discoveries that shape current ecological understanding of this poorly explored microbial habitat. Additionally, we highlight the need for multifaceted experimental approaches to observe phenomena such as cryptic cycles, complex interactions, and episymbiosis, which may not be apparent when using single approaches in isolation, but are nonetheless critical to advancing our understanding of this deep biosphere.</p>","PeriodicalId":50271,"journal":{"name":"ISME Journal","volume":" ","pages":""},"PeriodicalIF":10.8,"publicationDate":"2024-01-08","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11170664/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141082788","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"环境科学与生态学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
ISME JournalPub Date : 2024-01-08DOI: 10.1093/ismejo/wrae093
Ofer Kimchi, Yigal Meir, Ned S Wingreen
{"title":"Lytic and temperate phage naturally coexist in a dynamic population model.","authors":"Ofer Kimchi, Yigal Meir, Ned S Wingreen","doi":"10.1093/ismejo/wrae093","DOIUrl":"10.1093/ismejo/wrae093","url":null,"abstract":"<p><p>When phage infect their bacterial hosts, they may either lyse the cell and generate a burst of new phage, or lysogenize the bacterium, incorporating the phage genome into it. Phage lysis/lysogeny strategies are assumed to be highly optimized, with the optimal tradeoff depending on environmental conditions. However, in nature, phage of radically different lysis/lysogeny strategies coexist in the same environment, preying on the same bacteria. How can phage preying on the same bacteria coexist if one is more optimal than the other? Here, we address this conundrum within a modeling framework, simulating the population dynamics of communities of phage and their lysogens. We find that coexistence between phage of different lysis/lysogeny strategies is a natural outcome of chaotic population dynamics that arise within sufficiently diverse communities, which ensure no phage is able to absolutely dominate its competitors. Our results further suggest a bet-hedging mechanism at the level of the phage pan-genome, wherein obligate lytic (virulent) strains typically outcompete temperate strains, but also more readily fluctuate to extinction within a local community.</p>","PeriodicalId":50271,"journal":{"name":"ISME Journal","volume":" ","pages":""},"PeriodicalIF":10.8,"publicationDate":"2024-01-08","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11187991/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141181327","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"环境科学与生态学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Rumen microbiome-driven insight into bile acid metabolism and host metabolic regulation.","authors":"Boyan Zhang, Xianzhe Jiang, Yue Yu, Yimeng Cui, Wei Wang, Hailing Luo, Sokratis Stergiadis, Bing Wang","doi":"10.1093/ismejo/wrae098","DOIUrl":"10.1093/ismejo/wrae098","url":null,"abstract":"<p><p>Gut microbes play a crucial role in transforming primary bile acids (BAs) into secondary forms, which influence systemic metabolic processes. The rumen, a distinctive and critical microbial habitat in ruminants, boasts a diverse array of microbial species with multifaceted metabolic capabilities. There remains a gap in our understanding of BA metabolism within this ecosystem. Herein, through the analysis of 9371 metagenome-assembled genomes and 329 cultured organisms from the rumen, we identified two enzymes integral to BA metabolism: 3-dehydro-bile acid delta4,6-reductase (baiN) and the bile acid:Na + symporter family (BASS). Both in vitro and in vivo experiments were employed by introducing exogenous BAs. We revealed a transformation of BAs in rumen and found an enzyme cluster, including L-ribulose-5-phosphate 3-epimerase and dihydroorotate dehydrogenase. This cluster, distinct from the previously known BA-inducible operon responsible for 7α-dehydroxylation, suggests a previously unrecognized pathway potentially converting primary BAs into secondary BAs. Moreover, our in vivo experiments indicated that microbial BA administration in the rumen can modulate amino acid and lipid metabolism, with systemic impacts underscored by core secondary BAs and their metabolites. Our study provides insights into the rumen microbiome's role in BA metabolism, revealing a complex microbial pathway for BA biotransformation and its subsequent effect on host metabolic pathways, including those for glucose, amino acids, and lipids. This research not only advances our understanding of microbial BA metabolism but also underscores its wider implications for metabolic regulation, offering opportunities for improving animal and potentially human health.</p>","PeriodicalId":50271,"journal":{"name":"ISME Journal","volume":" ","pages":""},"PeriodicalIF":10.8,"publicationDate":"2024-01-08","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11193847/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141248862","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"环境科学与生态学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
ISME JournalPub Date : 2024-01-08DOI: 10.1093/ismejo/wrae096
Nataliya Teteneva, Ananda Sanches-Medeiros, Victor Sourjik
{"title":"Genome-wide screen of genetic determinants that govern Escherichia coli growth and persistence in lake water.","authors":"Nataliya Teteneva, Ananda Sanches-Medeiros, Victor Sourjik","doi":"10.1093/ismejo/wrae096","DOIUrl":"10.1093/ismejo/wrae096","url":null,"abstract":"<p><p>Although enteric bacteria normally reside within the animal intestine, the ability to persist extraintestinally is an essential part of their overall lifestyle, and it might contribute to transmission between hosts. Despite this potential importance, few genetic determinants of extraintestinal growth and survival have been identified, even for the best-studied model, Escherichia coli. In this work, we thus used a genome-wide library of barcoded transposon insertions to systematically identify functional clusters of genes that are crucial for E. coli fitness in lake water. Our results revealed that inactivation of pathways involved in maintaining outer membrane integrity, nucleotide biosynthesis, and chemotaxis negatively affected E. coli growth or survival in this extraintestinal environment. In contrast, inactivation of another group of genes apparently benefited E. coli growth or persistence in filtered lake water, resulting in higher abundance of these mutants. This group included rpoS, which encodes the general stress response sigma factor, as well as genes encoding several other global transcriptional regulators and RNA chaperones, along with several poorly annotated genes. Based on this co-enrichment, we identified these gene products as novel positive regulators of RpoS activity. We further observed that, despite their enhanced growth, E. coli mutants with inactive RpoS had reduced viability in lake water, and they were not enriched in the presence of the autochthonous microbiota. This highlights the duality of the general stress response pathway for E. coli growth outside the host.</p>","PeriodicalId":50271,"journal":{"name":"ISME Journal","volume":" ","pages":""},"PeriodicalIF":10.8,"publicationDate":"2024-01-08","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11188689/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141318821","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"环境科学与生态学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
ISME JournalPub Date : 2024-01-08DOI: 10.1093/ismejo/wrae126
Citlali Fonseca-García, Dean Pettinga, Andrew Wilson, Joshua R Elmore, Ryan McClure, Jackie Atim, Julie Pedraza, Robert Hutmacher, Halbay Turumtay, Yang Tian, Aymerick Eudes, Henrik V Scheller, Robert G Egbert, Devin Coleman-Derr
{"title":"Defined synthetic microbial communities colonize and benefit field-grown sorghum.","authors":"Citlali Fonseca-García, Dean Pettinga, Andrew Wilson, Joshua R Elmore, Ryan McClure, Jackie Atim, Julie Pedraza, Robert Hutmacher, Halbay Turumtay, Yang Tian, Aymerick Eudes, Henrik V Scheller, Robert G Egbert, Devin Coleman-Derr","doi":"10.1093/ismejo/wrae126","DOIUrl":"10.1093/ismejo/wrae126","url":null,"abstract":"<p><p>The rhizosphere constitutes a dynamic interface between plant hosts and their associated microbial communities. Despite the acknowledged potential for enhancing plant fitness by manipulating the rhizosphere, the engineering of the rhizosphere microbiome through inoculation has posed significant challenges. These challenges are thought to arise from the competitive microbial ecosystem where introduced microbes must survive, and the absence of adaptation to the specific metabolic and environmental demands of the rhizosphere. Here, we engineered a synthetic rhizosphere community (SRC1) with the anticipation that it would exhibit a selective advantage in colonizing the host Sorghum bicolor, thereby potentially fostering its growth. SRC1 was assembled from bacterial isolates identified either for their potential role in community cohesion through network analysis or for their ability to benefit from host-specific exudate compounds. The growth performance of SRC1 was assessed in vitro on solid media, in planta under gnotobiotic laboratory conditions, and in the field. Our findings reveal that SRC1 cohesion is most robust when cultivated in the presence of the plant host under laboratory conditions, with lineages being lost from the community when grown either in vitro or in a native field setting. We establish that SRC1 effectively promotes the growth of both above- and below-ground plant phenotypes in both laboratory and native field contexts. Furthermore, in laboratory conditions, these growth enhancements correlate with the transcriptional dampening of lignin biosynthesis in the host. Collectively, these results underscore the potential utility of synthetic microbial communities for modulating crop performance in controlled and native environments alike.</p>","PeriodicalId":50271,"journal":{"name":"ISME Journal","volume":" ","pages":""},"PeriodicalIF":10.8,"publicationDate":"2024-01-08","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11410050/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141565019","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"环境科学与生态学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
ISME JournalPub Date : 2024-01-08DOI: 10.1093/ismejo/wrae127
Zhe Pan, Yanhong Chen, Mi Zhou, Tim A McAllister, Tom N Mcneilly, Le Luo Guan
{"title":"Linking active rectal mucosa-attached microbiota to host immunity reveals its role in host-pathogenic STEC O157 interactions.","authors":"Zhe Pan, Yanhong Chen, Mi Zhou, Tim A McAllister, Tom N Mcneilly, Le Luo Guan","doi":"10.1093/ismejo/wrae127","DOIUrl":"10.1093/ismejo/wrae127","url":null,"abstract":"<p><p>The rectal-anal junction (RAJ) is the major colonization site of Shiga toxin-producing Escherichia coli (STEC) O157 in beef cattle, leading to transmission of this foodborne pathogen from farms to food chains. To date, there is limited understanding regarding whether the mucosa-attached microbiome has a profound impact on host-STEC interactions. In this study, the active RAJ mucosa-attached microbiota and its potential role in host immunity-STEC commensal interactions were investigated using RAJ mucosal biopsies collected from calves orally challenged with two STEC O157 strains with or without functional stx2a (stx2a+ or stx2a-). The results revealed that shifts of microbial diversity, topology, and assembly patterns were subjected to stx2a production post-challenge and Paeniclostridium and Gallibacterium were the keystone taxa for both microbial interactions and assembly. Additional mucosal transcriptome profiling showed stx2a-dependent host immune responses (i.e. B- and T-cell signaling and antigen processing and presentation) post-challenge. Further integrated analysis revealed that mucosa-attached beneficial microbes (i.e. Provotella, Faecalibacterium, and Dorea) interacted with host immune genes pre-challenge to maintain host homeostasis; however, opportunistic pathogenic microbes (i.e. Paeniclostridium) could interact with host immune genes after the STEC O157 colonization and interactions were stx2a-dependent. Furthermore, predicted bacterial functions involved in pathogen (O157 and Paeniclostridium) colonization and metabolism were related to host immunity. These findings suggest that during pathogen colonization, host-microbe interactions could shift from beneficial to opportunistic pathogenic bacteria driven and be dependent on the production of particular virulence factors, highlighting the potential regulatory role of mucosa-attached microbiota in affecting pathogen-commensal host interactions in calves with STEC O157 infection.</p>","PeriodicalId":50271,"journal":{"name":"ISME Journal","volume":" ","pages":""},"PeriodicalIF":10.8,"publicationDate":"2024-01-08","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11304501/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141565021","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"环境科学与生态学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Anaerobic ammonium oxidation coupled to iron(III) reduction catalyzed by a lithoautotrophic nitrate-reducing iron(II) oxidizing enrichment culture.","authors":"Hong-Bin Zhang, He-Fei Wang, Jia-Bo Liu, Zhen Bi, Ruo-Fei Jin, Tian Tian","doi":"10.1093/ismejo/wrae149","DOIUrl":"10.1093/ismejo/wrae149","url":null,"abstract":"<p><p>The last two decades have seen nitrogen/iron-transforming bacteria at the forefront of new biogeochemical discoveries, such as anaerobic ammonium oxidation coupled to ferric iron reduction (feammox) and lithoautotrophic nitrate-reducing ferrous iron-oxidation (NRFeOx). These emerging findings continue to expand our knowledge of the nitrogen/iron cycle in nature and also highlight the need to re-understand the functional traits of the microorganisms involved. Here, as a proof-of-principle, we report compelling evidence for the capability of an NRFeOx enrichment culture to catalyze the feammox process. Our results demonstrate that the NRFeOx culture predominantly oxidizes NH4+ to nitrogen gas, by reducing both chelated nitrilotriacetic acid (NTA)-Fe(III) and poorly soluble Fe(III)-bearing minerals (γ-FeOOH) at pH 4.0 and 8.0, respectively. In the NRFeOx culture, Fe(II)-oxidizing bacteria of Rhodanobacter and Fe(III)-reducing bacteria of unclassified_Acidobacteriota coexisted. Their relative abundances were dynamically regulated by the supplemented iron sources. Metagenomic analysis revealed that the NRFeOx culture contained a complete set of denitrifying genes along with hao genes for ammonium oxidation. Additionally, numerous genes encoding extracellular electron transport-associated proteins or their homologs were identified, which facilitated the reduction of extracellular iron by this culture. More broadly, this work lightens the unexplored potential of specific microbial groups in driving nitrogen transformation through multiple pathways and highlights the essential role of microbial iron metabolism in the integral biogeochemical nitrogen cycle.</p>","PeriodicalId":50271,"journal":{"name":"ISME Journal","volume":" ","pages":""},"PeriodicalIF":10.8,"publicationDate":"2024-01-08","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11366258/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141856963","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"环境科学与生态学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
ISME JournalPub Date : 2024-01-08DOI: 10.1093/ismejo/wrae033
Marcel Suleiman, Natalie Le Lay, Francesca Demaria, Boris A Kolvenbach, Mariana S Cretoiu, Owen L Petchey, Alexandre Jousset, Philippe F-X Corvini
{"title":"Pollutant profile complexity governs wastewater removal of recalcitrant pharmaceuticals.","authors":"Marcel Suleiman, Natalie Le Lay, Francesca Demaria, Boris A Kolvenbach, Mariana S Cretoiu, Owen L Petchey, Alexandre Jousset, Philippe F-X Corvini","doi":"10.1093/ismejo/wrae033","DOIUrl":"10.1093/ismejo/wrae033","url":null,"abstract":"<p><p>Organic pollutants are an increasing threat for wildlife and humans. Managing their removal is however complicated by the difficulties in predicting degradation rates. In this work, we demonstrate that the complexity of the pollutant profile, the set of co-existing contaminants, is a major driver of biodegradation in wastewater. We built representative assemblages out of one to five common pharmaceuticals (caffeine, atenolol, paracetamol, ibuprofen, and enalapril) selected along a gradient of biodegradability. We followed their individual removal by wastewater microbial communities. The presence of multichemical background pollution was essential for the removal of recalcitrant molecules such as ibuprofen. High-order interactions between multiple pollutants drove removal efficiency. We explain these interactions by shifts in the microbiome, with degradable molecules such as paracetamol enriching species and pathways involved in the removal of several organic pollutants. We conclude that pollutants should be treated as part of a complex system, with emerging pollutants potentially showing cascading effects and offering leverage to promote bioremediation.</p>","PeriodicalId":50271,"journal":{"name":"ISME Journal","volume":" ","pages":""},"PeriodicalIF":10.8,"publicationDate":"2024-01-08","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10989296/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"139998137","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"环境科学与生态学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}