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      Editorial: Actinobacteria in Special and Extreme Habitats: Diversity, Function Roles and Environmental Adaptations, Second Edition

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          Abstract

          Actinobacteria produce structurally diverse bioactive natural products, such as enzymes, antibiotics, antitumor and immune regulatory agents. Actinobacteria are not only the main producers of microbial-derived drugs, they also play an important role as symbionts in plant-associated microbial communities (Barka et al., 2015). At the same time, members of the phylum Actinobacteria were found to be widely distributed in different ecological environments, including diverse special and extreme habitats of aquatic and terrestrial ecosystem (Qin et al., 2011; Dhakal et al., 2017; Goodfellow et al., 2018). Compared with actinobacteria from temperate habitats, the community structure, diversity, biological activities, and mechanisms of environmental adaptation of those actinobacteria in special and extreme environments are relatively unstudied and unclear, and their functions and utilization are even less reported. These actinobacteria are potential new sources of novel natural products and functions for exploitation in medicine, agriculture, and industry. It's exciting that there are more and more reports in this field recently. These discoveries make us consider some intriguing and new questions, such as, are actinobacteria ubiquitous in the special and extreme environment on Earth, and where are the limits of their survival? At the same time, the discovery of more and more pure cultures and new taxa of actinobacteria from extreme environments has raised new questions for the taxonomy of the phylum Actinobacteria. How can we establish a more accurate taxonomic system to reflect the natural evolutionary relationship of Actinobacteria? Moreover, how can we recognize the specific ecological functions of these ecologically adapted actinobacteria and their potential unique environmental adaptation mechanisms? Following the success of the Research Topic, “Actinobacteria in special and extreme habitats: diversity, functional roles, and environmental adaptations” (Qin et al., 2016), organized in 2015, we are happy to launch a second edition. More than 100 authors, from 14 different countries, contributed a total of 16 articles in this new edition, including one review paper and 15 original research articles, covering a variety of topics related to actinobacteria in special and extreme habitats. These articles addressed issues related to the cultivation methods of rare actinobacteria, metagenomic analyses of diversity, phylogenomic taxonomy, genome mining, bioactive compounds, and their habitat adaptation mechanism using omics approaches. We are grateful to all authors who have submitted their manuscripts to the second edition of this Research Topic. The special and extreme environments are likely to contain abundant rare actinobacteria and novel species. However, the acquisition of pure culture is a prerequisite for the further study of their classification and function. Caves spread all over the world, being dark, humid, and nutrient-limited. The cultivation of these cave microorganisms has proven to be challenging (Ghosh et al., 2017). An original article by Fang et al. explores the effects of heat pretreatment, pH, and calcium salts on isolation of rare actinobacteria from Karstic Caves in Yunnan, China. A total of 204 isolates were cultured, and the authors obtained a high number of 29 different rare actinobacterial genera. Actinobacteria from caves have been found to produce a variety of secondary metabolites. However, studies of microbial ecology in caves are still very limited. Recently, members of actinobacteria were reported to be possibly involved in the moonmilk genesis (Bindschedler et al., 2014). Interestingly, the article by Maciejewska et al. provides novel evidences that some filamentous Streptomyces could be key protagonists in the genesis of moonmilk through a wide spectrum of biomineralization processes. These studies enlarged our knowledge on cave actinobacterial diversity and their special ecological functions. Desert is the most extreme non-polar biome on Earth. Recent metagenomic analyses of hyper-arid and extreme hyper-arid desert soils revealed a remarkable degree of actinobacterial “dark matter” (Idris et al., 2017). The diversity of actinobacterial taxa in the Badain Jaran (BJD) and Tengger Deserts (TGD) of China were assessed using combined cultivation-dependent and high-throughput sequencing techniques (Sun et al.). These authors found that the phylum Actinobacteria was the predominant, comprising 35.0 and 29.4% of the communities in the two desert sands, respectively. Taxonomic classification of 1,162 actinobacterial strains revealed a high diversity of 73 genera, including 37 new taxa, and 10.36 % of the tested isolates showed antimicrobial activities (Sun et al.). However, their ecological significance in deserts deserved further exploration. Marine actinobacteria have attracted more and more attention because of their special physiological characteristics and capacity of producing various natural compounds with diverse bioactivities (Schinke et al., 2017). However, marine actinobacteria producing anti-complement agents are still poorly explored. Xu et al. analyzed the genome of a marine Streptomyces sp. DUT11, which showed a strong anti-complement activity, and isolated the active compounds tunicamycins I, V, and VII. Another marine actinobacterium, Glycomyces sediminimaris UTMC 2460, which showed anti-microfouling activity, was analyzed for its active compounds. These authors concluded that diketopiperazines produced by this strain could be used as environmentally safe anti-fouling agents to prevent the fouling process in marine habitats (Heidarian et al.). The article by Sun et al. reveals the marine adaptation mechanism of a sponge-derived actinobacterium, Kocuria flava S43, by comparative genomics analysis. These authors found that gene acquisition was probably a primary mechanism of environmental adaptation in K. flava S43 (Sun et al.). These studies indicated that marine actinobacteria are rich sources of diverse biological compounds. In this Research Topic, we collected five papers related to endophytic actinobacteria, which is also a research hotspot in recent years. Habitat-adapted, symbiotic, indigenous endophytic actinobacteria from special and extreme habitats probably contain novel taxa and compounds, and enhance their host tolerance of harsh environments (Mesa et al., 2017; Qin et al., 2018). The article by Singh and Dubey reviews the taxonomic and chemical diversity of endophytic actinobacteria in arid, mangrove, non-mangrove saline and aquatic ecosystems and discusses their potential biotechnological applications. Similarly, Jiang et al. explores the diversity and antibacterial activities of endophytic actinobacteria from five different mangrove plants in Guangxi Zhuang Autonomous Region, China; they found 28 actinobacterial genera and four potential new species. The two articles by Bibi et al. and Wei et al. report on the endophytic actinobacteria and their biological secondary metabolites from the halophyte Salsola imbricate and Chinese tea plants; their results confirm again that endophytic actinobacteria might be an undeveloped bioresource library for active compounds. Lasudee et al. report the actinobacteria associated with arbuscular mycorrhizal spores of Funneliformis mosseae, and explore their potential plant growth promotion effects in agriculture; results showed that the isolates could produce indole-3-acetic acid (IAA) and siderophores, solubilize phosphate, and promote rice plant growth. Genome sequencing and the phylogenomic strategy have been explored for the research of taxonomy and prokaryotic systematics. For instance, the class Acidimicrobiia is comprised of few cultivable species at present, containing only the order Acidimicrobiales, two families Acidimicrobiaceae and Iamiaceae with few genera (Ludwig et al., 2012). Hu et al. analyzed 20 sequenced members of this class and identified 15 conserved signature indels (CSIs) in widely distributed proteins and 26 conserved signature proteins (CSPs); the phylogenomic analysis revealed another three major lineages in addition to the two recognized families. Furthermore, Sangal et al. revisit the taxonomic status of the biomedically and industrially important genus Amycolatopsis, using a phylogenomic approach. According to the genome sequences analysis and the core genome phylogeny, genus Amycolatopsis was subdivided into four major clades and several singletons (Sangal et al.). These results indicate that whole genome sequencing analysis can provide more accurate taxonomic status for prokaryotes. The developments of omics methods have provided a robust support for our understanding of the actinobacterial adaptation mechanisms to the special and extreme habitats. Cornell et al. obtained 76 plasmid-containing isolates of actinomycetes from the Great Salt Plains of Oklahoma. Eleven isolates were chosen for genome sequencing, and the results revealed the presence of series genes involved in antibiotic production, antibiotic, and heavy metal resistance, osmoregulation, and stress response, which likely facilitate their survival in the extreme halophilic environment (Cornell et al.). By transcriptome analysis, physiological, and molecular experiments, Han et al. found that accumulation of ectoine played a vital role for the salt stress tolerance of the halotolerant Nocardiopsis gilva YIM 90087T. The article by Yin et al. report that a hybrid strategy was used to utilize carbon sources at different temperatures by an aerobic, and cellulose degrading thermophilic actinomycete, Thermoactinospora rubra YIM 77501T, by using combined genomic and transcriptomics methods. In summary, this Research Topic second edition presents recent discoveries on diversity, function roles, and environmental adaptations of actinobacteria in special and extreme habitats; and broadens our knowledge of actinobacterial diversity and their ecophysiological function. We are delighted to present this Research Topic in Frontiers in Microbiology. We hope that readers of the Journal will not only enjoy this Research Topic but also will find it a useful reference. Future research still looks forward to the innovation and application of new technologies, such as the application of single cell microfluidic technique to obtain new pure cultures. At the same time, the cooperation of different disciplines, and international cooperation of scientists from different countries should be strengthened. We also believe that in the future, more “dark matter” from actinobacteria in special and extreme environments will be discovered and utilized for the benefit of human beings. Author Contributions W-JL and SQ organized this topic. SQ wrote the editorial article. H-PK, WH, and IA are co-editors of the topic and discussed the writing. Conflict of Interest Statement The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

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          Biodiversity, bioactive natural products and biotechnological potential of plant-associated endophytic actinobacteria.

          Endophytic actinobacteria, which exist in the inner tissues of living plants, have attracted increasing attention among taxonomists, ecologists, agronomists, chemists and evolutionary biologists. Numerous studies have indicated that these prolific actinobacteria appear to have a capacity to produce an impressive array of secondary metabolites exhibiting a wide variety of biological activity, such as antibiotics, antitumor and anti-infection agents, plant growth promoters and enzymes, and may contribute to their host plants by promoting growth and enhancing their ability of withstanding the environmental stresses. These microorganisms may represent an underexplored reservoir of novel species of potential interest in the discovery of novel lead compounds and for exploitation in pharmaceutical, agriculture and industry. This review focuses on new findings in the isolation methods, bio- and chemical diversity of endophytic actinobacteria and reveals the potential biotechnological application. The facing problems and strategies for biodiversity research and bioactive natural products producing are also discussed.
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            Marine Rare Actinobacteria: Isolation, Characterization, and Strategies for Harnessing Bioactive Compounds

            Actinobacteria are prolific producers of thousands of biologically active natural compounds with diverse activities. More than half of these bioactive compounds have been isolated from members belonging to actinobacteria. Recently, rare actinobacteria existing at different environmental settings such as high altitudes, volcanic areas, and marine environment have attracted attention. It has been speculated that physiological or biochemical pressures under such harsh environmental conditions can lead to the production of diversified natural compounds. Hence, marine environment has been focused for the discovery of novel natural products with biological potency. Many novel and promising bioactive compounds with versatile medicinal, industrial, or agricultural uses have been isolated and characterized. The natural compounds cannot be directly used as drug or other purposes, so they are structurally modified and diversified to ameliorate their biological or chemical properties. Versatile synthetic biological tools, metabolic engineering techniques, and chemical synthesis platform can be used to assist such structural modification. This review summarizes the latest studies on marine rare actinobacteria and their natural products with focus on recent approaches for structural and functional diversification of such microbial chemicals for attaining better applications.
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              Diversity of Bacterial Microbiota of Coastal Halophyte Limonium sinense and Amelioration of Salinity Stress Damage by Symbiotic Plant Growth-Promoting Actinobacterium Glutamicibacter halophytocola KLBMP 5180

              Plant-associated microorganisms are considered a key determinant of plant health and growth. However, little information is available regarding the composition and ecological function of the roots' and leaves' bacterial microbiota of halophytes. Here, using both culture-dependent and culture-independent techniques, we characterized the bacterial communities of the roots and leaves as well as the rhizosphere and bulk soils of the coastal halophyte Limonium sinense in Jiangsu Province, China. We identified 49 representative bacterial strains belonging to 17 genera across all samples, with Glutamicibacter as the most dominant genus. All Glutamicibacter isolates showed multiple potential plant growth promotion traits and tolerated a high concentration of NaCl and a wide pH range. Interestingly, further inoculation experiments showed that the Glutamicibacter halophytocola strain KLBMP 5180 isolated from root tissue significantly promoted host growth under NaCl stress. Indeed, KLBMP 5180 inoculation increased the concentrations of total chlorophyll, proline, antioxidative enzymes, flavonoids, K + , and Ca 2+ in the leaves; the concentrations of malondialdehyde (MDA) and Na + were reduced. A transcriptome analysis identified 1,359 and 328 differentially expressed genes (DEGs) in inoculated seedlings treated with 0 and 250 mM NaCl, respectively. We found that pathways related to phenylpropanoid and flavonoid biosynthesis and ion transport and metabolism might play more important roles in host salt stress tolerance induced by KLBMP 5180 inoculation compared to that in noninoculated leaves. Our results provide novel insights into the complex composition and function of the bacterial microbiota of the coastal halophyte L. sinense and suggest that halophytes might recruit specific bacteria to enhance their tolerance of harsh environments. IMPORTANCE Halophytes are important coastal plants often used for the remediation of saline coastal soils. Limonium sinense is well known for its medical properties and phytoremediation of saline soils. However, excessive exploitation and utilization have made the wild resource endangered. The use of endophytic and rhizosphere bacteria may be one of the suitable ways to solve the problem. This study was undertaken to develop approaches to improve the growth of L. sinense using endophytes. The application of actinobacterial endophytes ameliorated salt stress damage of the host via complex physiological and molecular mechanisms. The results also highlight the potential of using habitat-adapted, symbiotic, indigenous endophytic bacteria to enhance the growth and ameliorate abiotic stress damage of host plants growing in special habitats.
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                Author and article information

                Contributors
                Journal
                Front Microbiol
                Front Microbiol
                Front. Microbiol.
                Frontiers in Microbiology
                Frontiers Media S.A.
                1664-302X
                30 April 2019
                2019
                : 10
                : 944
                Affiliations
                [1] 1The Key Laboratory of Biotechnology for Medicinal Plant of Jiangsu Province, Jiangsu Normal University , Xuzhou, China
                [2] 2State Key Laboratory of Biocontrol and Guangdong Provincial Key Laboratory of Plant Resources, School of Life Sciences, Sun Yat-sen University , Guangzhou, China
                [3] 3Southern Laboratory of Ocean Science and Engineering (Guangdong, Zhuhai) , Zhuhai, China
                [4] 4School of Natural and Environmental Sciences, Newcastle University , Newcastle upon Tyne, United Kingdom
                [5] 5Bioproducts Research Chair, Zoology Department, College of Science, King Saud University , Riyadh, Saudi Arabia
                [6] 6Botany and Microbiology Department, Faculty of Science, Beni-Suef University , Beni-Suef, Egypt
                [7] 7National Agricultural Research Center, Bio-resources Conservation Institute , Islamabad, Pakistan
                Author notes

                Edited by: Don A. Cowan, University of Pretoria, South Africa

                Reviewed by: Alan Bull, University of Kent, United Kingdom

                *Correspondence: Sheng Qin shengqin@ 123456jsnu.edu.cn

                This article was submitted to Extreme Microbiology, a section of the journal Frontiers in Microbiology

                Article
                10.3389/fmicb.2019.00944
                6503213
                31114567
                1a419ce0-0f5c-42fb-a9cc-adabc6a4ca46
                Copyright © 2019 Qin, Li, Klenk, Hozzein and Ahmed.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 31 January 2019
                : 15 April 2019
                Page count
                Figures: 0, Tables: 0, Equations: 0, References: 12, Pages: 3, Words: 2463
                Categories
                Microbiology
                Editorial

                Microbiology & Virology
                actinobacteria,special and extreme environments,diversity,omics technologies,phylogenomics,activities,environmental adaptation

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