Pub Date : 2023-12-20Epub Date: 2023-11-29DOI: 10.1128/mmbr.00186-21
Buzz Baum, Anja Spang
SUMMARYIn this hypothesis article, we explore the origin of the eukaryotic nucleus. In doing so, we first look afresh at the nature of this defining feature of the eukaryotic cell and its core functions-emphasizing the utility of seeing the eukaryotic nucleoplasm and cytoplasm as distinct regions of a common compartment. We then discuss recent progress in understanding the evolution of the eukaryotic cell from archaeal and bacterial ancestors, focusing on phylogenetic and experimental data which have revealed that many eukaryotic machines with nuclear activities have archaeal counterparts. In addition, we review the literature describing the cell biology of representatives of the TACK and Asgardarchaeaota - the closest known living archaeal relatives of eukaryotes. Finally, bringing these strands together, we propose a model for the archaeal origin of the nucleus that explains much of the current data, including predictions that can be used to put the model to the test.
{"title":"On the origin of the nucleus: a hypothesis.","authors":"Buzz Baum, Anja Spang","doi":"10.1128/mmbr.00186-21","DOIUrl":"10.1128/mmbr.00186-21","url":null,"abstract":"<p><p>SUMMARYIn this hypothesis article, we explore the origin of the eukaryotic nucleus. In doing so, we first look afresh at the nature of this defining feature of the eukaryotic cell and its core functions-emphasizing the utility of seeing the eukaryotic nucleoplasm and cytoplasm as distinct regions of a common compartment. We then discuss recent progress in understanding the evolution of the eukaryotic cell from archaeal and bacterial ancestors, focusing on phylogenetic and experimental data which have revealed that many eukaryotic machines with nuclear activities have archaeal counterparts. In addition, we review the literature describing the cell biology of representatives of the TACK and Asgardarchaeaota - the closest known living archaeal relatives of eukaryotes. Finally, bringing these strands together, we propose a model for the archaeal origin of the nucleus that explains much of the current data, including predictions that can be used to put the model to the test.</p>","PeriodicalId":18520,"journal":{"name":"Microbiology and Molecular Biology Reviews","volume":" ","pages":"e0018621"},"PeriodicalIF":12.9,"publicationDate":"2023-12-20","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10732040/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"138451931","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2023-12-20Epub Date: 2023-11-27DOI: 10.1128/mmbr.00184-22
Mireille Bétermier, Lawrence A Klobutcher, Eduardo Orias
SUMMARYCiliated protozoa undergo large-scale developmental rearrangement of their somatic genomes when forming a new transcriptionally active macronucleus during conjugation. This process includes the fragmentation of chromosomes derived from the germline, coupled with the efficient healing of the broken ends by de novo telomere addition. Here, we review what is known of developmental chromosome fragmentation in ciliates that have been well-studied at the molecular level (Tetrahymena, Paramecium, Euplotes, Stylonychia, and Oxytricha). These organisms differ substantially in the fidelity and precision of their fragmentation systems, as well as in the presence or absence of well-defined sequence elements that direct excision, suggesting that chromosome fragmentation systems have evolved multiple times and/or have been significantly altered during ciliate evolution. We propose a two-stage model for the evolution of the current ciliate systems, with both stages involving repetitive or transposable elements in the genome. The ancestral form of chromosome fragmentation is proposed to have been derived from the ciliate small RNA/chromatin modification process that removes transposons and other repetitive elements from the macronuclear genome during development. The evolution of this ancestral system is suggested to have potentiated its replacement in some ciliate lineages by subsequent fragmentation systems derived from mobile genetic elements.
{"title":"Programmed chromosome fragmentation in ciliated protozoa: multiple means to chromosome ends.","authors":"Mireille Bétermier, Lawrence A Klobutcher, Eduardo Orias","doi":"10.1128/mmbr.00184-22","DOIUrl":"10.1128/mmbr.00184-22","url":null,"abstract":"<p><p>SUMMARYCiliated protozoa undergo large-scale developmental rearrangement of their somatic genomes when forming a new transcriptionally active macronucleus during conjugation. This process includes the fragmentation of chromosomes derived from the germline, coupled with the efficient healing of the broken ends by <i>de novo</i> telomere addition. Here, we review what is known of developmental chromosome fragmentation in ciliates that have been well-studied at the molecular level (<i>Tetrahymena</i>, <i>Paramecium</i>, <i>Euplotes</i>, <i>Stylonychia</i>, and <i>Oxytricha</i>). These organisms differ substantially in the fidelity and precision of their fragmentation systems, as well as in the presence or absence of well-defined sequence elements that direct excision, suggesting that chromosome fragmentation systems have evolved multiple times and/or have been significantly altered during ciliate evolution. We propose a two-stage model for the evolution of the current ciliate systems, with both stages involving repetitive or transposable elements in the genome. The ancestral form of chromosome fragmentation is proposed to have been derived from the ciliate small RNA/chromatin modification process that removes transposons and other repetitive elements from the macronuclear genome during development. The evolution of this ancestral system is suggested to have potentiated its replacement in some ciliate lineages by subsequent fragmentation systems derived from mobile genetic elements.</p>","PeriodicalId":18520,"journal":{"name":"Microbiology and Molecular Biology Reviews","volume":" ","pages":"e0018422"},"PeriodicalIF":8.0,"publicationDate":"2023-12-20","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10732028/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"138445289","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2023-12-20Epub Date: 2023-11-14DOI: 10.1128/mmbr.00174-22
Katherine L Cotten, Kimberly Michele Davis
SUMMARYAntibiotic persistence, or the ability of small subsets of bacteria to survive prolonged antibiotic treatment, is an underappreciated cause of antibiotic treatment failure. Over the past decade, researchers have discovered multiple different stress responses and mechanisms that can promote antibiotic persistence. However, many of these studies have been completed in culture-based systems that fail to truly replicate the complexities of the host environment, and it is unclear whether the mechanisms defined in in vitro studies are applicable during host infection. In this review, we focus our discussion on recent studies that utilize a mixture of ex vivo culture systems and animal models to understand what stressors in the host environment are important for inducing antibiotic persistence. Different host stressors are involved depending on the anatomical niche the bacteria reside in and whether the host immune system is primed to generate a more robust response against bacteria, which can result in differing downstream effects on antibiotic susceptibility. Bacterial pathogens can also utilize specific strategies to reprogram their metabolism, which is vital for transitioning into an antibiotic-persistent state within host tissues. Importantly, we highlight that more attention is needed to establish guidelines for in vivo work on antibiotic persistence, particularly when identifying antibiotic-persistent subpopulations and distinguishing these phenotypes from antibiotic tolerance. Studying antibiotic persistence in the context of the host environment will be crucial for developing tools and strategies to target antibiotic-persistent bacteria and increase the efficacy of antibiotic treatment.
{"title":"Bacterial heterogeneity and antibiotic persistence: bacterial mechanisms utilized in the host environment.","authors":"Katherine L Cotten, Kimberly Michele Davis","doi":"10.1128/mmbr.00174-22","DOIUrl":"10.1128/mmbr.00174-22","url":null,"abstract":"<p><p>SUMMARYAntibiotic persistence, or the ability of small subsets of bacteria to survive prolonged antibiotic treatment, is an underappreciated cause of antibiotic treatment failure. Over the past decade, researchers have discovered multiple different stress responses and mechanisms that can promote antibiotic persistence. However, many of these studies have been completed in culture-based systems that fail to truly replicate the complexities of the host environment, and it is unclear whether the mechanisms defined in <i>in vitro</i> studies are applicable during host infection. In this review, we focus our discussion on recent studies that utilize a mixture of <i>ex vivo</i> culture systems and animal models to understand what stressors in the host environment are important for inducing antibiotic persistence. Different host stressors are involved depending on the anatomical niche the bacteria reside in and whether the host immune system is primed to generate a more robust response against bacteria, which can result in differing downstream effects on antibiotic susceptibility. Bacterial pathogens can also utilize specific strategies to reprogram their metabolism, which is vital for transitioning into an antibiotic-persistent state within host tissues. Importantly, we highlight that more attention is needed to establish guidelines for <i>in vivo</i> work on antibiotic persistence, particularly when identifying antibiotic-persistent subpopulations and distinguishing these phenotypes from antibiotic tolerance. Studying antibiotic persistence in the context of the host environment will be crucial for developing tools and strategies to target antibiotic-persistent bacteria and increase the efficacy of antibiotic treatment.</p>","PeriodicalId":18520,"journal":{"name":"Microbiology and Molecular Biology Reviews","volume":" ","pages":"e0017422"},"PeriodicalIF":5.4,"publicationDate":"2023-12-20","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10732018/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"92155196","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2023-12-20Epub Date: 2023-10-16DOI: 10.1128/mmbr.00103-23
Huifang Zhu, Chunfu Zheng
{"title":"Correction for Zhu and Zheng, \"The Race between Host Antiviral Innate Immunity and the Immune Evasion Strategies of Herpes Simplex Virus 1\".","authors":"Huifang Zhu, Chunfu Zheng","doi":"10.1128/mmbr.00103-23","DOIUrl":"10.1128/mmbr.00103-23","url":null,"abstract":"","PeriodicalId":18520,"journal":{"name":"Microbiology and Molecular Biology Reviews","volume":" ","pages":"e0010323"},"PeriodicalIF":12.9,"publicationDate":"2023-12-20","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10732015/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"41236759","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2023-12-20Epub Date: 2023-12-04DOI: 10.1128/mmbr.00041-23
Susan K Amundsen, Gerald R Smith
SUMMARYRecBCD enzyme is a multi-functional protein that initiates the major pathway of homologous genetic recombination and DNA double-strand break repair in Escherichia coli. It is also required for high cell viability and aids proper DNA replication. This 330-kDa, three-subunit enzyme is one of the fastest, most processive helicases known and contains a potent nuclease controlled by Chi sites, hotspots of recombination, in DNA. RecBCD undergoes major changes in activity and conformation when, during DNA unwinding, it encounters Chi (5'-GCTGGTGG-3') and nicks DNA nearby. Here, we discuss the multitude of mutations in each subunit that affect one or another activity of RecBCD and its control by Chi. These mutants have given deep insights into how the multiple activities of this complex enzyme are coordinated and how it acts in living cells. Similar studies could help reveal how other complex enzymes are controlled by inter-subunit interactions and conformational changes.
{"title":"RecBCD enzyme: mechanistic insights from mutants of a complex helicase-nuclease.","authors":"Susan K Amundsen, Gerald R Smith","doi":"10.1128/mmbr.00041-23","DOIUrl":"10.1128/mmbr.00041-23","url":null,"abstract":"<p><p>SUMMARYRecBCD enzyme is a multi-functional protein that initiates the major pathway of homologous genetic recombination and DNA double-strand break repair in <i>Escherichia coli</i>. It is also required for high cell viability and aids proper DNA replication. This 330-kDa, three-subunit enzyme is one of the fastest, most processive helicases known and contains a potent nuclease controlled by Chi sites, hotspots of recombination, in DNA. RecBCD undergoes major changes in activity and conformation when, during DNA unwinding, it encounters Chi (5'-GCTGGTGG-3') and nicks DNA nearby. Here, we discuss the multitude of mutations in each subunit that affect one or another activity of RecBCD and its control by Chi. These mutants have given deep insights into how the multiple activities of this complex enzyme are coordinated and how it acts in living cells. Similar studies could help reveal how other complex enzymes are controlled by inter-subunit interactions and conformational changes.</p>","PeriodicalId":18520,"journal":{"name":"Microbiology and Molecular Biology Reviews","volume":" ","pages":"e0004123"},"PeriodicalIF":8.0,"publicationDate":"2023-12-20","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10732027/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"138478066","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2023-12-20Epub Date: 2023-11-01DOI: 10.1128/mmbr.00048-23
Angelique E Ray, Dana Z Tribbia, Don A Cowan, Belinda C Ferrari
Summary: Atmospheric chemosynthesis is a recently proposed form of chemoautotrophic microbial primary production. The proposed process relies on the oxidation of trace concentrations of hydrogen (≤530 ppbv), carbon monoxide (≤90 ppbv), and methane (≤1,870 ppbv) gases using high-affinity enzymes. Atmospheric hydrogen and carbon monoxide oxidation have been primarily linked to microbial growth in desert surface soils scarce in liquid water and organic nutrients, and low in photosynthetic communities. It is well established that the oxidation of trace hydrogen and carbon monoxide gases widely supports the persistence of microbial communities in a diminished metabolic state, with the former potentially providing a reliable source of metabolic water. Microbial atmospheric methane oxidation also occurs in oligotrophic desert soils and is widespread throughout copiotrophic environments, with established links to microbial growth. Despite these findings, the direct link between trace gas oxidation and carbon fixation remains disputable. Here, we review the supporting evidence, outlining major gaps in our understanding of this phenomenon, and propose approaches to validate atmospheric chemosynthesis as a primary production process. We also explore the implications of this minimalistic survival strategy in terms of nutrient cycling, climate change, aerobiology, and astrobiology.
{"title":"Clearing the air: unraveling past and guiding future research in atmospheric chemosynthesis.","authors":"Angelique E Ray, Dana Z Tribbia, Don A Cowan, Belinda C Ferrari","doi":"10.1128/mmbr.00048-23","DOIUrl":"10.1128/mmbr.00048-23","url":null,"abstract":"<p><strong>Summary: </strong>Atmospheric chemosynthesis is a recently proposed form of chemoautotrophic microbial primary production. The proposed process relies on the oxidation of trace concentrations of hydrogen (≤530 ppbv), carbon monoxide (≤90 ppbv), and methane (≤1,870 ppbv) gases using high-affinity enzymes. Atmospheric hydrogen and carbon monoxide oxidation have been primarily linked to microbial growth in desert surface soils scarce in liquid water and organic nutrients, and low in photosynthetic communities. It is well established that the oxidation of trace hydrogen and carbon monoxide gases widely supports the persistence of microbial communities in a diminished metabolic state, with the former potentially providing a reliable source of metabolic water. Microbial atmospheric methane oxidation also occurs in oligotrophic desert soils and is widespread throughout copiotrophic environments, with established links to microbial growth. Despite these findings, the direct link between trace gas oxidation and carbon fixation remains disputable. Here, we review the supporting evidence, outlining major gaps in our understanding of this phenomenon, and propose approaches to validate atmospheric chemosynthesis as a primary production process. We also explore the implications of this minimalistic survival strategy in terms of nutrient cycling, climate change, aerobiology, and astrobiology.</p>","PeriodicalId":18520,"journal":{"name":"Microbiology and Molecular Biology Reviews","volume":" ","pages":"e0004823"},"PeriodicalIF":8.0,"publicationDate":"2023-12-20","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10732025/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"71424891","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2023-12-20Epub Date: 2023-09-26DOI: 10.1128/mmbr.00082-23
Kimberly R Sabsay, Aartjan J W Te Velthuis
SUMMARYNegative and ambisense RNA viruses are the causative agents of important human diseases such as influenza, measles, Lassa fever, and Ebola hemorrhagic fever. The viral genome of these RNA viruses consists of one or more single-stranded RNA molecules that are encapsidated by viral nucleocapsid proteins to form a ribonucleoprotein complex (RNP). This RNP acts as protection, as a scaffold for RNA folding, and as the context for viral replication and transcription by a viral RNA polymerase. However, the roles of the viral nucleoproteins extend beyond these functions during the viral infection cycle. Recent advances in structural biology techniques and analysis methods have provided new insights into the formation, function, dynamics, and evolution of negative sense virus nucleocapsid proteins, as well as the role that they play in host innate immune responses against viral infection. In this review, we discuss the various roles of nucleocapsid proteins, both in the context of RNPs and in RNA-free states, as well as the open questions that remain.
{"title":"Negative and ambisense RNA virus ribonucleocapsids: more than protective armor.","authors":"Kimberly R Sabsay, Aartjan J W Te Velthuis","doi":"10.1128/mmbr.00082-23","DOIUrl":"10.1128/mmbr.00082-23","url":null,"abstract":"<p><p>SUMMARYNegative and ambisense RNA viruses are the causative agents of important human diseases such as influenza, measles, Lassa fever, and Ebola hemorrhagic fever. The viral genome of these RNA viruses consists of one or more single-stranded RNA molecules that are encapsidated by viral nucleocapsid proteins to form a ribonucleoprotein complex (RNP). This RNP acts as protection, as a scaffold for RNA folding, and as the context for viral replication and transcription by a viral RNA polymerase. However, the roles of the viral nucleoproteins extend beyond these functions during the viral infection cycle. Recent advances in structural biology techniques and analysis methods have provided new insights into the formation, function, dynamics, and evolution of negative sense virus nucleocapsid proteins, as well as the role that they play in host innate immune responses against viral infection. In this review, we discuss the various roles of nucleocapsid proteins, both in the context of RNPs and in RNA-free states, as well as the open questions that remain.</p>","PeriodicalId":18520,"journal":{"name":"Microbiology and Molecular Biology Reviews","volume":" ","pages":"e0008223"},"PeriodicalIF":8.0,"publicationDate":"2023-12-20","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10732063/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"41150881","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2023-12-20Epub Date: 2023-12-04DOI: 10.1128/mmbr.00121-21
Megan S Hill, Jack A Gilbert
SUMMARYOver the past decade, hundreds of studies have characterized the microbial communities found in human-associated built environments (BEs). These have focused primarily on how the design and use of our built spaces have shaped human-microbe interactions and how the differential selection of certain taxa or genetic traits has influenced health outcomes. It is now known that the more removed humans are from the natural environment, the greater the risk for the development of autoimmune and allergic diseases, and that indoor spaces can be harsh, selective environments that can increase the emergence of antimicrobial-resistant and virulent phenotypes in surface-bound communities. However, despite the abundance of research that now points to the importance of BEs in determining human-microbe interactions, only a fraction of non-human animal structures have been comparatively explored. It is here, in the context of human-associated BE research, that we consider the microbial ecology of animal-built natural nests and burrows, as well as artificial enclosures, and point to areas of primary interest for future research.
{"title":"Microbiology of the built environment: harnessing human-associated built environment research to inform the study and design of animal nests and enclosures.","authors":"Megan S Hill, Jack A Gilbert","doi":"10.1128/mmbr.00121-21","DOIUrl":"10.1128/mmbr.00121-21","url":null,"abstract":"<p><p>SUMMARYOver the past decade, hundreds of studies have characterized the microbial communities found in human-associated built environments (BEs). These have focused primarily on how the design and use of our built spaces have shaped human-microbe interactions and how the differential selection of certain taxa or genetic traits has influenced health outcomes. It is now known that the more removed humans are from the natural environment, the greater the risk for the development of autoimmune and allergic diseases, and that indoor spaces can be harsh, selective environments that can increase the emergence of antimicrobial-resistant and virulent phenotypes in surface-bound communities. However, despite the abundance of research that now points to the importance of BEs in determining human-microbe interactions, only a fraction of non-human animal structures have been comparatively explored. It is here, in the context of human-associated BE research, that we consider the microbial ecology of animal-built natural nests and burrows, as well as artificial enclosures, and point to areas of primary interest for future research.</p>","PeriodicalId":18520,"journal":{"name":"Microbiology and Molecular Biology Reviews","volume":" ","pages":"e0012121"},"PeriodicalIF":8.0,"publicationDate":"2023-12-20","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10732082/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"138478065","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}