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      A New Front in Microbial Warfare—Delivery of Antifungal Effectors by the Type VI Secretion System

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          Abstract

          Microbes typically exist in mixed communities and display complex synergistic and antagonistic interactions. The Type VI secretion system (T6SS) is widespread in Gram-negative bacteria and represents a contractile nano-machine that can fire effector proteins directly into neighbouring cells. The primary role assigned to the T6SS is to function as a potent weapon during inter-bacterial competition, delivering antibacterial effectors into rival bacterial cells. However, it has recently emerged that the T6SS can also be used as a powerful weapon against fungal competitors, and the first fungal-specific T6SS effector proteins, Tfe1 and Tfe2, have been identified. These effectors act via distinct mechanisms against a variety of fungal species to cause cell death. Tfe1 intoxication triggers plasma membrane depolarisation, whilst Tfe2 disrupts nutrient uptake and induces autophagy. Based on the frequent coexistence of bacteria and fungi in microbial communities, we propose that T6SS-dependent antifungal activity is likely to be widespread and elicited by a suite of antifungal effectors. Supporting this hypothesis, homologues of Tfe1 and Tfe2 are found in other bacterial species, and a number of T6SS-elaborating species have been demonstrated to interact with fungi. Thus, we envisage that antifungal T6SS will shape many polymicrobial communities, including the human microbiota and disease-causing infections.

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          Most cited references43

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          Living in a fungal world: impact of fungi on soil bacterial niche development.

          The colonization of land by plants appears to have coincided with the appearance of mycorrhiza-like fungi. Over evolutionary time, fungi have maintained their prominent role in the formation of mycorrhizal associations. In addition, however, they have been able to occupy other terrestrial niches of which the decomposition of recalcitrant organic matter is perhaps the most remarkable. This implies that, in contrast to that of aquatic organic matter decomposition, bacteria have not been able to monopolize decomposition processes in terrestrial ecosystems. The emergence of fungi in terrestrial ecosystems must have had a strong impact on the evolution of terrestrial bacteria. On the one hand, potential decomposition niches, e.g. lignin degradation, have been lost for bacteria, whereas on the other hand the presence of fungi has itself created new bacterial niches. Confrontation between bacteria and fungi is ongoing, and from studying contemporary interactions, we can learn about the impact that fungi presently have, and have had in the past, on the ecology and evolution of terrestrial bacteria. In the first part of this review, the focus is on niche differentiation between soil bacteria and fungi involved in the decomposition of plant-derived organic matter. Bacteria and fungi are seen to compete for simple plant-derived substrates and have developed antagonistic strategies. For more recalcitrant organic substrates, e.g. cellulose and lignin, both competitive and mutualistic strategies appear to have evolved. In the second part of the review, bacterial niches with respect to the utilization of fungal-derived substrates are considered. Here, several lines of development can be recognized, ranging from mutualistic exudate-consuming bacteria that are associated with fungal surfaces to endosymbiotic and mycophagous bacteria. In some cases, there are indications of fungal specific selection in fungus-associated bacteria, and possible mechanisms for such selection are discussed.
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            Serratia infections: from military experiments to current practice.

            Serratia species, in particular Serratia marcescens, are significant human pathogens. S. marcescens has a long and interesting taxonomic, medical experimentation, military experimentation, and human clinical infection history. The organisms in this genus, particularly S. marcescens, were long thought to be nonpathogenic. Because S. marcescens was thought to be a nonpathogen and is usually red pigmented, the U.S. military conducted experiments that attempted to ascertain the spread of this organism released over large areas. In the process, members of both the public and the military were exposed to S. marcescens, and this was uncovered by the press in the 1970s, leading to U.S. congressional hearings. S. marcescens was found to be a certain human pathogen by the mid-1960s. S. marcescens and S. liquefaciens have been isolated as causative agents of numerous outbreaks and opportunistic infections, and the association of these organisms with point sources such as medical devices and various solutions given to hospitalized patients is striking. Serratia species appear to be common environmental organisms, and this helps to explain the large number of nosocomial infections due to these bacteria. Since many nosocomial infections are caused by multiply antibiotic-resistant strains of S. marcescens, this increases the danger to hospitalized patients, and hospital personnel should be vigilant in preventing nosocomial outbreaks due to this organism. S. marcescens, and probably other species in the genus, carries several antibiotic resistance determinants and is also capable of acquiring resistance genes. S. marcescens and S. liquefaciens are usually identified well in the clinical laboratory, but the other species are rare enough that laboratory technologists may not recognize them. 16S rRNA gene sequencing may enable better identification of some of the less common Serratia species.
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              Medically important bacterial-fungal interactions.

              Whether it is in the setting of disease or in a healthy state, the human body contains a diverse range of microorganisms, including bacteria and fungi. The interactions between these taxonomically diverse microorganisms are highly dynamic and dependent on a multitude of microorganism and host factors. Human disease can develop from an imbalance between commensal bacteria and fungi or from invasion of particular host niches by opportunistic bacterial and fungal pathogens. This Review describes the clinical and molecular characteristics of bacterial-fungal interactions that are relevant to human disease.
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                Author and article information

                Journal
                J Fungi (Basel)
                J Fungi (Basel)
                jof
                Journal of Fungi
                MDPI
                2309-608X
                14 June 2019
                June 2019
                : 5
                : 2
                : 50
                Affiliations
                [1 ]Institute for Cell and Molecular Biosciences, Faculty of Medicine, Newcastle University, Newcastle upon Tyne NE2 4HH, UK; katharina.trunk@ 123456ncl.ac.uk
                [2 ]Division of Molecular Microbiology, School of Life Sciences, University of Dundee, Dundee DD1 5EH, UK
                Author notes
                [* ]Correspondence: s.j.coulthurst@ 123456dundee.ac.uk (S.J.C.); janet.quinn@ 123456ncl.ac.uk (J.Q.); Tel.: +44-(0)1382-86208 (S.J.C.); +44-(0)191-2087434 (J.Q.)
                Article
                jof-05-00050
                10.3390/jof5020050
                6617251
                31197124
                955ee18e-f558-4f4f-9e5c-b3089f6daa30
                © 2019 by the authors.

                Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license ( http://creativecommons.org/licenses/by/4.0/).

                History
                : 17 May 2019
                : 13 June 2019
                Categories
                Review

                type vi secretion system,polymicrobial interactions,antifungal effectors

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