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John A. Fuerst - One of the best experts on this subject based on the ideXlab platform.
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Planctomycetes new models for microbial cells and activities
Microbial Resources#R##N#From Functional Existence in Nature to Applications, 2017Co-Authors: John A. FuerstAbstract:Planctomycetes are a unique divergent phylum of the domain Bacteria. Members display a number of unusual properties, such as cell compartmentalization among many species examined electron microscopically, the presence of unusual or unique lipids, such as sterols and ladderane lipids in some species, and unique physiology in some species, such as the anammox Planctomycetes performing ammonium oxidation anaerobically. This chapter will outline their diversity, examine planctomycete cell compartmentalization as a new model for cell complexity and activities, and outline the potential of planctomycete species to be considered significant new microbial resources, including sources for new lipids and enzymes, and for new types of waste remediation technology on industrial scales utilizing the anammox process unique to Planctomycetes.
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Correspondence
2015Co-Authors: Margaret K Butler, John A. FuerstAbstract:The Planctomycetes, order Planctomycetales, are a distinct phylum of domain Bacteria. Genes encoding the RNA portion of ribonuclease P (RNase P) of some planctomycete members were sequenced and compared with existing database planctomycete sequences. rnpB gene sequences encoding RNase P RNA were generated by a conserved primer PCR strategy for Planctomyces brasiliensis, Planctomyces limnophilus, Pirellula marina, Pirellula staleyi strain ATCC 35122, Isosphaera pallida, one other Isosphaera strain, Gemmata obscuriglobus and three other strains of the Gemmata group. These sequences were aligned against reference bacterial sequences and secondary structures of corresponding RNase P RNAs deduced by a comparative approach. P12 helices were found to be highly variable in length, as were helices P16.1 and P19, when present. RNase P RNA secondary structures of Gemmata isolates were found to have unusual features relative to other Planctomycetes, including a long P9 helix and an insert in the P13 helix not found in any other member of domain Bacteria. These unique features are consistent with other unusual properties of this genus, distinguishing it from other bacteria. Phylogenetic analyses indicate that relationships between Planctomycetes derived from RNase P RNA are consistent with 16S rRNA-based analyses
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structural studies of planctomycete gemmata obscuriglobus support cell compartmentalisation in a bacterium
PLOS ONE, 2014Co-Authors: Evgeny Sagulenko, Richard I Webb, Garry P Morgan, John A. FuerstAbstract:Members of phylum Planctomycetes have been proposed to possess atypical cell organisation for the Bacteria, having a structure of sectioned cells consistent with internal compartments surrounded by membranes. Here via electron tomography we confirm the presence of compartments in the planctomycete Gemmata obscuriglobus cells. Resulting 3-D models for the most prominent structures, nuclear body and riboplasm, demonstrate their entirely membrane - enclosed nature. Immunogold localization of the FtsK protein also supports the internal organisation of G.obscuriglobus cells and their unique mechanism of cell division. We discuss how these new data expand our knowledge on bacterial cell biology and suggest evolutionary consequences of the findings.
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Isolation and diversity of Planctomycetes from the sponge Niphates sp., seawater, and sediment of Moreton Bay, Australia
Antonie van Leeuwenhoek, 2013Co-Authors: Hiroshi Izumi, Richard I Webb, Evgeny Sagulenko, John A. FuerstAbstract:Planctomycetes are ubiquitous in marine environment and were reported to occur in association with multicellular eukaryotic organisms such as marine macroalgae and invertebrates. Here, we investigate Planctomycetes associated with the marine sponge Niphates sp. from the sub-tropical Australian coast by assessing their diversity using culture-dependent and -independent approaches based on the 16S rRNA gene. The culture-dependent approach resulted in the isolation of a large collection of diverse Planctomycetes including some novel lineages of Planctomycetes from the sponge as well as sediment and seawater of Moreton Bay where this sponge occurs. The characterization of these novel Planctomycetes revealed that cells of one unique strain do not possess condensed nucleoids, a phenotype distinct from other Planctomycetes. In addition, a culture-independent clone library approach identified unique planctomycete 16S rRNA gene sequences closely related to other sponge-derived sequences. The analysis of tissue of the sponge Niphates sp. showed that the mesohyl of the sponge is almost devoid of microbial cells, indicating this species is in the group of ‘low microbial abundant’ (LMA) sponges. The unique planctomycete 16S rRNA gene sequences identified in this study were phylogenetically closely related to sequences from LMA sponges in other published studies. This study has revealed new insights into the diversity of Planctomycetes in the marine environment and the association of Planctomycetes with marine sponges.
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Nested Bacterial Boxes: Nuclear and Other Intracellular Compartments in Planctomycetes
Journal of Molecular Microbiology and Biotechnology, 2013Co-Authors: John A. Fuerst, Evgeny SagulenkoAbstract:Bacteria in the phylum Planctomycetes and some related phyla challenge our concept of the typical bacterium as consisting of cells without internal compartments or membrane-bounded organelles. Cells of all species of Planctomycetes examined consist of at least two major compartments, and there are two other types of compartmentation in which a third compartment is formed either by a double-membrane envelope around the nucleoid in the case of the aerobic Gemmata obscuriglobus or by a single but potentially energized membrane in the case of the anaerobic ammonium-oxidizing anammox Planctomycetes. We examine here the nature of these planctomycete compartments in relation to function and their relationship to the endomembranes defining them, and discuss the implications of the remarkable compartment-confined process of protein uptake in Gemmata, which resembles receptor- and clathrin-mediated endocytosis of eukaryotes. Planctomycetes have implications for our understanding of the evolution of membrane-bounded organelles, of endomembranes, transport across endomembranes and membrane trafficking, and for how the complexity of a eukaryote style of cell organization could have originated.
Damien P. Devos - One of the best experts on this subject based on the ideXlab platform.
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Thalassoglobus polymorphus sp. nov., a novel Planctomycete isolated close to a public beach of Mallorca Island
Antonie van Leeuwenhoek, 2020Co-Authors: Elena Rivas-marin, Christian Boedeker, Mareike Jogler, Mike S M Jetten, Anja Heuer, Sandra Wiegand, Nicolai Kallscheuer, Stijn H. Peeters, Manfred Rohde, Damien P. DevosAbstract:Access to axenic cultures is crucial to extend the knowledge of the biology, lifestyle or metabolic capabilities of bacteria from different phyla. The phylum Planctomycetes is an excellent example since its members display an unusual cell biology and complex lifestyles. As a contribution to the current collection of axenic planctomycete cultures, here we describe strain Mal48^T isolated from phytoplankton material sampled at the coast of S’Arenal close to Palma de Mallorca (Spain). The isolated strain shows optimal growth at pH 7.0–7.5 and 30 °C and exhibits typical features of Planctomycetes. Cells of the strain are spherical to pear-shaped, divide by polar budding with daughter cells showing the same shape as the mother cell, tend to aggregate, display a stalk and produce matrix or fimbriae. Strain Mal48^T showed 95.8% 16S rRNA gene sequence similarity with the recently described Thalassoglobus neptunius KOR42^T. The genome sequence of the novel isolate has a size of 6,357,355 bp with a G+C content of 50.3%. A total of 4874 protein-coding genes, 41 tRNA genes and 2 copies of the 16S rRNA gene are encoded in the genome. Based on phylogenetic, morphological and physiological analyses, we conclude that strain Mal48^T (= DSM 100737^T = LMG 29019^T) should be classified as the type strain of a new species in the genus Thalassoglobus , for which the name Thalassoglobus polymorphus sp. nov. is proposed.
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essentiality of sterol synthesis genes in the planctomycete bacterium gemmata obscuriglobus
Nature Communications, 2019Co-Authors: Elena Rivasmarin, Sean Stettner, Ekaterina Y Gottshall, Mitch Helling, Carlos Santanamolina, Naomi L Ward, Franco Basile, Damien P. DevosAbstract:Sterols and hopanoids are chemically and structurally related lipids mostly found in eukaryotic and bacterial cell membranes. Few bacterial species have been reported to produce sterols and this anomaly had originally been ascribed to lateral gene transfer (LGT) from eukaryotes. In addition, the functions of sterols in these bacteria are unknown and the functional overlap between sterols and hopanoids is still unclear. Gemmata obscuriglobus is a bacterium from the Planctomycetes phylum that synthesizes sterols, in contrast to its hopanoid-producing relatives. Here we show that sterols are essential for growth of G. obscuriglobus, and that sterol depletion leads to aberrant membrane structures and defects in budding cell division. This report of sterol essentiality in a prokaryotic species advances our understanding of sterol distribution and function, and provides a foundation to pursue fundamental questions in evolutionary cell biology. Sterols play essential functions in eukaryotic cell membranes, but are produced by few bacterial species. Here, the authors show that they are essential for growth of the planctomycete bacterium Gemmata obscuriglobus.
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determining the bacterial cell biology of Planctomycetes
Nature Communications, 2017Co-Authors: Christian Boedeker, Muriel C. F. Van Teeseling, Margarete Schuler, Greta Reintjes, Olga Jeske, Mareike Jogler, Patrick Rast, Daniela Borchert, Damien P. DevosAbstract:Bacteria of the phylum Planctomycetes have been previously reported to possess several features that are typical of eukaryotes, such as cytosolic compartmentalization and endocytosis-like macromolecule uptake. However, recent evidence points towards a Gram-negative cell plan for Planctomycetes, although in-depth experimental analysis has been hampered by insufficient genetic tools. Here we develop methods for expression of fluorescent proteins and for gene deletion in a model planctomycete, Planctopirus limnophila, to analyse its cell organization in detail. Super-resolution light microscopy of mutants, cryo-electron tomography, bioinformatic predictions and proteomic analyses support an altered Gram-negative cell plan for Planctomycetes, including a defined outer membrane, a periplasmic space that can be greatly enlarged and convoluted, and an energized cytoplasmic membrane. These conclusions are further supported by experiments performed with two other Planctomycetes, Gemmata obscuriglobus and Rhodopirellula baltica. We also provide experimental evidence that is inconsistent with endocytosis-like macromolecule uptake; instead, extracellular macromolecules can be taken up and accumulate in the periplasmic space through unclear mechanisms.
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development of genetic tools for the manipulation of the Planctomycetes
Frontiers in Microbiology, 2016Co-Authors: Elena Rivasmarin, Ines Canosa, Eduardo Santero, Damien P. DevosAbstract:Bacteria belonging to the Planctomycetes, Verrucomicrobia, Chlamydiae (PVC) superphylum are of interest for biotechnology, evolutionary cell biology, ecology and human health. Some PVC species lack a number of typical bacterial features while others possess characteristics that are usually more associated to eukaryotes or archaea. For example, the Planctomycetes phylum is atypical for the absence of the FtsZ protein and for the presence of a developed endomembrane system. Studies of the cellular and molecular biology of these infrequent characteristics are currently limited due to the lack of genetic tools for most of the species. So far, genetic manipulation in Planctomycetes has been described in Planctopirus limnophila only. Here we show a simple approach that allows mutagenesis by homologous recombination in three different Planctomycetes species (i.e. Gemmata obscuriglobus, Gimesia maris and Blastopirellula marina), in addition to P. limnophila, thus extending the repertoire of genetically modifiable organisms in this superphylum. Although the Planctomycetes show high resistance to most antibiotics, we have used kanamycin resistance genes in G. obscuriglobus, P. limnophila and G. maris, and tetracycline resistance genes in B. marina, as markers for mutant selection. In all cases, plasmids were introduced in the strains by mating or electroporation, and the genetic modification was verified by Southern Blotting analysis. In addition we show that the green fluorescent protein (gfp) is expressed in all four backgrounds from an Escherichia coli promoter. The genetic manipulation achievement in four phylogenetically diverse Planctomycetes will enable molecular studies in these strains, and opens the door to developing genetic approaches not only in other Planctomycetes but also other species of the superphylum, such as the Lentisphaerae.
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endocytosis like protein uptake in the bacterium gemmata obscuriglobus
Proceedings of the National Academy of Sciences of the United States of America, 2010Co-Authors: Thierry G A Lonhienne, Josef D Franke, Richard I Webb, Evgeny Sagulenko, Bernard J Carroll, Amanda Nouwens, Damien P. Devos, John A. FuerstAbstract:Endocytosis is a process by which extracellular material such as macromolecules can be incorporated into cells via a membrane-trafficking system. Although universal among eukaryotes, endocytosis has not been identified in Bacteria or Archaea. However, intracellular membranes are known to compartmentalize cells of bacteria in the phylum Planctomycetes, suggesting the potential for endocytosis and membrane trafficking in members of this phylum. Here we show that cells of the planctomycete Gemmata obscuriglobus have the ability to uptake proteins present in the external milieu in an energy-dependent process analogous to eukaryotic endocytosis, and that internalized proteins are associated with vesicle membranes. Occurrence of such ability in a bacterium is consistent with autogenous evolution of endocytosis and the endomembrane system in an ancestral noneukaryote cell.
Svetlana N Dedysh - One of the best experts on this subject based on the ideXlab platform.
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wide distribution of phycisphaera like Planctomycetes from wd2101 soil group in peatlands and genome analysis of the first cultivated representative
Environmental Microbiology, 2021Co-Authors: Svetlana N Dedysh, Irina S Kulichevskaya, Anastasia A. Ivanova, Alexey V Beletsky, Natalia E Suzina, D A Philippov, Andrey L Rakitin, Andrey V Mardanov, Nikolai V RavinAbstract:Phycisphaera-like WD2101 'soil group' is one of the as-yet-uncultivated phylogenetic clades within the phylum Planctomycetes. Members of this clade are commonly detected in various terrestrial habitats. This study shows that WD2101 represented one of the major planctomycete groups in 10 boreal peatlands, comprising up to 76% and 36% of all Planctomycetes-affiliated 16S rRNA gene reads in raised bogs and eutrophic fens respectively. These types of peatlands displayed clearly distinct intra-group diversity of WD2101-affiliated Planctomycetes. The first isolate of this enigmatic planctomycete group, strain M1803, was obtained from a humic lake surrounded by Sphagnum peat bogs. Strain M1803 displayed 89.2% 16S rRNA gene similarity to Tepidisphaera mucosa and was represented by motile cocci that divided by binary fission and grew under micro-oxic conditions. The complete 7.19 Mb genome of strain M1803 contained an array of genes encoding Planctomycetal type bacterial microcompartment organelle likely involved in l-rhamnose metabolism, suggesting participation of M1803-like Planctomycetes in polysaccharide degradation in peatlands. The corresponding cellular microcompartments were revealed in ultrathin cell sections. Strain M1803 was classified as a novel genus and species, Humisphaera borealis gen. nov., sp. nov., affiliated with the formerly recognized WD2101 'soil group'.
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lacipirellula parvula gen nov sp nov representing a lineage of Planctomycetes widespread in low oxygen habitats description of the family lacipirellulaceae fam nov and proposal of the orders pirellulales ord nov gemmatales ord nov and isosphaerales ord nov
Systematic and Applied Microbiology, 2020Co-Authors: Svetlana N Dedysh, Irina S Kulichevskaya, Anastasia A. Ivanova, Irene W C Rijpstra, Alexey V Beletsky, Andrey V Mardanov, Jaap Sinninghe S Damste, Nikolai V RavinAbstract:Abstract Pirellula-like Planctomycetes are ubiquitous aquatic bacteria, which are often detected in anoxic or micro-oxic habitats. By contrast, the taxonomically described representatives of these bacteria, with very few exceptions, are strict aerobes. Here, we report the isolation and characterization of the facultatively anaerobic planctomycete, strain PX69T, which was isolated from a boreal lake. Its 16S rRNA gene sequence is affiliated with the Pirellula-related Pir4 clade, which is dominated by environmental sequences retrieved from a variety of low-oxygen habitats. Strain PX69T was represented by ellipsoidal cells that multiplied by budding and grew on sugars, some polysaccharides and glycerol. Anaerobic growth occurred by means of fermentation. Strain PX69T grew at pH 5.5–7.5 and at temperatures between 10 and 30 °C. The major fatty acids were C18:1ω9c, C16:0 and C16:1ω7c; the major intact polar lipid was dimethylphosphatidylethanolamine. The complete genome of strain PX69T was 6.92 Mb in size; DNA G + C content was 61.7 mol%. Among characterized Planctomycetes, the highest 16S rRNA gene similarity (90.4%) was observed with ‘Bythopirellula goksoyri’ Pr1d, a planctomycete from deep-sea sediments. We propose to classify PX69T as a novel genus and species, Lacipirellula parvula gen. nov., sp. nov.; the type strain is strain PX69T (=KCTC 72398T = CECT 9826T = VKM B-3335T). This genus is placed in a novel family, Lacipirellulaceae fam. nov., which belongs to the order Pirellulales ord. nov. Based on the results of comparative genome analysis, we also suggest establishment of the orders Gemmatales ord. nov. and Isosphaerales ord. nov. as well as an emendation of the order Planctomycetales.
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Planctomycetes in boreal and subarctic wetlands diversity patterns and potential ecological functions
FEMS Microbiology Ecology, 2019Co-Authors: Svetlana N Dedysh, Anastasia A. IvanovaAbstract:Members of the phylum Planctomycetes are common inhabitants of boreal Sphagnum peat bogs and lichen-dominated tundra wetlands. These bacteria colonize both oxic and anoxic peat layers and reach the population size of 107 cells per gram of wet peat. The 16S rRNA gene sequences from Planctomycetes comprise 5%-22% of total 16S rRNA gene reads retrieved from peat samples. Most abundant peat-inhabiting Planctomycetes affiliate with the families Isosphaeraceae and Gemmataceae, and with as-yet-uncultured Phycisphaera-related group WD2101. The use of metatranscriptomics to assess the functional role of Planctomycetes in peatlands suggested the presence of versatile hydrolytic capabilities in these bacteria. This evidence was further confirmed by the analysis of genome-encoded capabilities of isolates from wetlands. Large (up to 12 Mbp) genomes of Planctomycetes encode wide repertoires of carbohydrate-active enzymes including many unclassified putative glycoside hydrolases, which suggests the presence of extremely high glycolytic potential in these bacteria. Experimental tests confirmed their ability to grow on xylan, pectin, starch, lichenan, cellulose, chitin and polysaccharides of microbial origin. These results provide an insight into the ecological roles of peat-inhabiting Planctomycetes and suggest their participation in degradation of plant-derived polymers, exoskeletons of peat-inhabiting arthropods as well as exopolysaccharides produced by other bacteria.
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Metatranscriptomics reveals the hydrolytic potential of peat-inhabiting Planctomycetes
Antonie van Leeuwenhoek, 2018Co-Authors: Anastasia A. Ivanova, Werner Liesack, Carl-eric Wegner, Svetlana N DedyshAbstract:Members of the phylum Planctomycetes are common inhabitants of northern Sphagnum -dominated wetlands. Evidence is accumulating that, in these environments, some Planctomycetes may be involved in degrading polymeric organic matter. The experimental data, however, remain scarce due to the low number of characterized representatives of this phylum. In a previous study, we used metatranscriptomics to assess the activity response of peat-inhabiting microorganisms to biopolymers abundantly present in native peat. The community responses to cellulose, xylan, pectin, and chitin availability were analysed relative to unamended controls. Here, we re-analysed these metatranscriptomes and retrieved a total of 1,602,783 rRNA and 35,522 mRNA sequences affiliated with the Planctomycetes . Each of the four polymers induced specific planctomycete responses. These were most pronounced on chitin. The two groups with increased 16S rRNA transcript pools were Gemmata - and Phycisphaera -like Planctomycetes. Among uncultivated members of the Planctomycetaceae , two increased transcript pools were detected in pectin-amended samples and belonged to Pirellula -like bacteria. The analysis of taxonomically assigned mRNA reads confirmed the specific response of Gemmata -related Planctomycetes to chitin amendment suggesting the presence of chitinolytic capabilities in these bacteria.
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distinct diversity patterns of Planctomycetes associated with the freshwater macrophyte nuphar lutea l smith
Antonie Van Leeuwenhoek International Journal of General and Molecular Microbiology, 2018Co-Authors: Anastasia A. Ivanova, Irina S Kulichevskaya, Dmitriy A Philippov, Svetlana N DedyshAbstract:Members of the phylum Planctomycetes were originally described as freshwater bacteria. Most recent studies, however, address planctomycete diversity in other environments colonized by these microorganisms, including marine and terrestrial ecosystems. This study was initiated in order to revisit the specific patterns of planctomycete diversity in freshwater habitats using cultivation-independent approaches. The specific focus was made on Planctomycetes associated with Nuphar lutea (L.) Smith, an emergent macrophyte with floating leaves, which is widespread in the Holarctic. As revealed by Illumina pair-end sequencing of 16S rRNA gene fragments, the bacterial assemblages colonizing floating leaf blades of waterlilies sampled from two different boreal lakes displayed similar composition but were distinct from the planktonic bacterial communities. 16S rRNA gene fragments from the Planctomycetes comprised 0.1–1 and 1–2.2% of total 16S rRNA gene reads retrieved from water samples and plant leaves, respectively. Planktonic Planctomycetes were mostly affiliated with the class Planctomycetaceae (77–97%), while members of the Phycisphaerae were less abundant (3–22%). The relative proportion of the latter group, however, increased by 13–45% on leaves of N. lutea. The Phycisphaera-related group WD2101, Pirellula-like Planctomycetes, as well as Gemmata, Zavarzinella and Planctopirus species were the most abundant groups of Planctomycetes associated with plant leaves, which may suggest their involvement in the degradation of plant-derived organic matter.
Mareike Jogler - One of the best experts on this subject based on the ideXlab platform.
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Thalassoglobus polymorphus sp. nov., a novel Planctomycete isolated close to a public beach of Mallorca Island
Antonie van Leeuwenhoek, 2020Co-Authors: Elena Rivas-marin, Christian Boedeker, Mareike Jogler, Mike S M Jetten, Anja Heuer, Sandra Wiegand, Nicolai Kallscheuer, Stijn H. Peeters, Manfred Rohde, Damien P. DevosAbstract:Access to axenic cultures is crucial to extend the knowledge of the biology, lifestyle or metabolic capabilities of bacteria from different phyla. The phylum Planctomycetes is an excellent example since its members display an unusual cell biology and complex lifestyles. As a contribution to the current collection of axenic planctomycete cultures, here we describe strain Mal48^T isolated from phytoplankton material sampled at the coast of S’Arenal close to Palma de Mallorca (Spain). The isolated strain shows optimal growth at pH 7.0–7.5 and 30 °C and exhibits typical features of Planctomycetes. Cells of the strain are spherical to pear-shaped, divide by polar budding with daughter cells showing the same shape as the mother cell, tend to aggregate, display a stalk and produce matrix or fimbriae. Strain Mal48^T showed 95.8% 16S rRNA gene sequence similarity with the recently described Thalassoglobus neptunius KOR42^T. The genome sequence of the novel isolate has a size of 6,357,355 bp with a G+C content of 50.3%. A total of 4874 protein-coding genes, 41 tRNA genes and 2 copies of the 16S rRNA gene are encoded in the genome. Based on phylogenetic, morphological and physiological analyses, we conclude that strain Mal48^T (= DSM 100737^T = LMG 29019^T) should be classified as the type strain of a new species in the genus Thalassoglobus , for which the name Thalassoglobus polymorphus sp. nov. is proposed.
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on the maverick Planctomycetes
Fems Microbiology Reviews, 2018Co-Authors: Sandra Wiegand, Mareike Jogler, Christian JoglerAbstract:Planctomycetes are ubiquitous, environmentally and biotechnologically important bacteria that are key players in global carbon and nitrogen cycles. Ever since their first discovery in the 1920s they seemed to blur the prokaryote /eukaryote dichotomy. After initially being described as fungi and reclassified as bacteria later, they were still thought to feature a nucleus-like compartment surrounding their highly condensed DNA. Also, an endocytosis-like uptake mechanism for macromolecules was described. Besides these eukaryotic hallmark traits, Planctomycetes seemed to lack typical bacterial features such as a peptidoglycan cell wall or the universal bacterial cell division protein FtsZ, while mostly dividing by polar budding instead of binary fission. Thus, Planctomycetes were speculated to be ancestral to both, bacteria and eukaryotes. With the advent of novel microscopic techniques, along with the development of genetic tools for Planctomycetes, some of these hypotheses were revisited. Surprisingly, Planctomycetes were found to possess a peptidoglycan cell wall and to comprise a cell plan comparable to other Gram-negative bacteria as the nucleus-like structure is rather an invagination of the cytoplasmic membrane than a cohesive compartment. These finding challenge the idea of a eukaryotic ancestry of the phylum, as Planctomycetes now appear similar, yet distinct to other bacteria.
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determining the bacterial cell biology of Planctomycetes
Nature Communications, 2017Co-Authors: Christian Boedeker, Muriel C. F. Van Teeseling, Margarete Schuler, Greta Reintjes, Olga Jeske, Mareike Jogler, Patrick Rast, Daniela Borchert, Damien P. DevosAbstract:Bacteria of the phylum Planctomycetes have been previously reported to possess several features that are typical of eukaryotes, such as cytosolic compartmentalization and endocytosis-like macromolecule uptake. However, recent evidence points towards a Gram-negative cell plan for Planctomycetes, although in-depth experimental analysis has been hampered by insufficient genetic tools. Here we develop methods for expression of fluorescent proteins and for gene deletion in a model planctomycete, Planctopirus limnophila, to analyse its cell organization in detail. Super-resolution light microscopy of mutants, cryo-electron tomography, bioinformatic predictions and proteomic analyses support an altered Gram-negative cell plan for Planctomycetes, including a defined outer membrane, a periplasmic space that can be greatly enlarged and convoluted, and an energized cytoplasmic membrane. These conclusions are further supported by experiments performed with two other Planctomycetes, Gemmata obscuriglobus and Rhodopirellula baltica. We also provide experimental evidence that is inconsistent with endocytosis-like macromolecule uptake; instead, extracellular macromolecules can be taken up and accumulate in the periplasmic space through unclear mechanisms.
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fuerstia marisgermanicae gen nov sp nov an unusual member of the phylum Planctomycetes from the german wadden sea
Frontiers in Microbiology, 2016Co-Authors: Timo Kohn, Christian Boedeker, Mareike Jogler, Patrick Rast, Daniela Borchert, Anja Heuer, John Vollmers, Boyke Bunk, Ines Glockner, Heike M FreeseAbstract:Members of the phylum Planctomycetes are ubiquitous bacteria that dwell in aquatic and terrestrial habitats. While planctomycetal species are important players in the global carbon- and nitrogen cycle, this phylum is still undersampled and only few genome sequences are available. Here we describe strain NH11T, a novel planctomycete obtained from a crustacean shell (Wadden Sea, Germany). The phylogenetically closest related cultivated species is Gimesia maris, sharing only 87% 16S rRNA sequence identity. Previous isolation attempts have mostly yielded members of the genus Rhodopirellula from water of the German North Sea. On the other hand, only one axenic culture of the genus Pirellula was obtained from a crustacean thus far. However, the 16S rRNA gene sequence of strain NH11T shares only 80% sequence identity with the closest relative of both genera, Rhodopirellula and Pirellula.. Thus, strain NH11T is unique in terms of origin and phylogeny. While the pear to ovoid shaped cells of strain NH11T are typical planctomycetal, light- and electron microscopic observations point towards an unusual variation of cell division through budding: during the division process daughter- and mother cells are connected by an unseen thin tubular-like structure. Furthermore, the periplasmic space of strain NH11T was unusually enlarged and differed from previously known Planctomycetes. The complete genome of strain NH11T, with almost 9 Mb in size, is among the largest planctomycetal genomes sequenced thus far, but harbors only 6645 protein-coding genes. The acquisition of genomic components by horizontal gene transfer is indicated by the presence of numerous putative genomic islands. Strikingly, 45 ‘giant-genes’ were found within the genome of NH11T. Subsequent analysis of all available planctomycetal genomes revealed that Planctomycetes as such are especially rich in ‘giant genes’. Furthermore, Multilocus Sequence Analysis (MLSA) tree reconstruction support the phylogenetic distance of strain NH11T from other cultivated Planctomycetes of the same phylogenetic cluster. Thus, based on our findings, we propose to classify strain NH11T as Fuerstia marisgermanicae gen. nov., sp. nov., with the type strain NH11T, within the phylum Planctomycetes.
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developing techniques for the utilization of Planctomycetes as producers of bioactive molecules
Frontiers in Microbiology, 2016Co-Authors: Olga Jeske, Mareike Jogler, Patrick Rast, Frank Surup, Marcel Kettenis, Birthe Forster, Joachim Wink, Christian JoglerAbstract:Planctomycetes are conspicuous, ubiquitous, environmentally important bacteria. They can attach to various surfaces in aquatic habitats and form biofilms. Their unique FtsZ-independent budding cell division mechanism is associated with slow growth and doubling times from six hours up to one month. Despite this putative disadvantage in the struggle to colonize surfaces, Planctomycetes are frequently associated with aquatic phototrophic organisms such as diatoms, cyanobacteria or kelp, whereby Planctomycetes can account for up to 50 % of the biofilm-forming bacterial population. Consequently, Planctomycetes were postulated to play an important role in carbon utilization, for example as scavengers after phototrophic blooms. However, given their observed slow growth, such findings are surprising since other faster- growing heterotrophs tend to colonize similar ecological niches. Accordingly, Planctomycetes were suspected to produce antibiotics for habitat protection in response to the attachment on phototrophs. Recently, we demonstrated their genomic potential to produce nonribosomal peptides, polyketides, bacteriocins, and terpenoids that might have antibiotic activities. In this study, we describe the development of a pipeline that consists of tools and procedures to cultivate Planctomycetes for the production of antimicrobial compounds in a chemically- defined medium and a procedure to chemically mimic their interaction with bacteria such as for example Cyanobacteria. We evaluated and adjusted screening assays to allow the hunt for planctomycetal antibiotics. As proof of principle, we demonstrate antimicrobial activities of planctomycetal extracts from Planctopirus limnophila DSM 3776, Rhodopirellula baltica DSM 10527, and the recently isolated strain Pan216. By combining UV/Vis and high resolution mass spectrometry data from High-Performance Liquid Chromatography fractionations with growth inhibition of indicator strains, we were able to assign the antibiotic activity to candidate peaks related to planctomycetal antimicrobial compounds. The MS analysis points towards the production of novel bioactive molecules with novel structures. Consequently, we developed a large scale cultivation procedure to allow future structural elucidation of such compounds. Our findings might have implications for the discovery of novel antibiotics as Planctomycetes represent a yet untapped resource that could be developed by employing the tools and methods described in this study.
Lise Ovreas - One of the best experts on this subject based on the ideXlab platform.
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Planctomycetes as a Vital Constituent of the Microbial Communities Inhabiting Different Layers of the Meromictic Lake Sælenvannet (Norway).
Microorganisms, 2020Co-Authors: Julia E. Storesund, Anders Lanzén, Eva-lena Nordmann, Hilde Rief Armo, Olga Maria Lage, Lise OvreasAbstract:Meromictic lakes are permanently stratified lakes that display steep gradients in salinity, oxygen and sulphur compounds tightly linked to bacterial community structure and diversity. Lake Saelenvannet is a meromictic lake located south of Bergen, Norway. The 26 m deep lake is connected to the open sea and permanently stratified into two layers separated by a chemocline. The upper water layer is brackish with major input from water runoff from the surroundings. The bottom layer consists of old saline water with low or no oxygen concentrations. Bacteria from phylum Planctomycetes are reported to be ubiquitous in lake environments. They are involved in the degradation of complex carbon sources in aquatic environments and are also linked to anaerobic processes such as fermentation and sulphur reduction. To study Planctomycete distribution along a chemical gradient, we sampled the water column throughout Lake Saelenvannet in 2012 and profiled the microbial community using 16S rRNA amplicon sequencing (metabarcoding) with 454 pyrosequencing. Planctomycetes related 16S rRNA gene sequences were found to be present both in the oxic and anoxic parts of the lake and showed an uneven distribution throughout the water column, with the highest relative abundance of 10% found in the saline anoxic layer at 15 m depth. In a follow-up study in 2014, samples from eight different depths were collected for enrichment and isolation of novel Planctomycetes. This study resulted in successful isolation in pure culture of 10 isolates affiliated to four different genera from the family Planctomycetaceae. One strain closely related to Blastopirellula cremea was isolated from 9 m depth, and two novel strains affiliated to the genera Stieleria and Gimesia were isolated at 7 and 9 m depths, respectively. Furthermore, seven isolates with identical 16S rRNA gene sequences were retrieved from seven different depths which varied greatly in salinity and chemical composition. These isolates likely represent a new species affiliated to Rubinisphaera. The adaptation of this novel Planctomycete to water depths spanning the entire chemical gradient could indicate a high phenotypic plasticity and/or a very efficient survival strategy. Overall, our results show the presence of a diverse group of Planctomycetes in Lake Saelenvannet, with a strong potential for novel adaptations to chemical stress factors.
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Diversity of Planctomycetes in iron-hydroxide deposits from the Arctic Mid Ocean Ridge (AMOR) and description of Bythopirellula goksoyri gen. nov., sp. nov., a novel Planctomycete from deep sea iron-hydroxide deposits.
Antonie Van Leeuwenhoek International Journal of General and Molecular Microbiology, 2013Co-Authors: Julia E. Storesund, Lise OvreasAbstract:Planctomycetes form a deep branching and distinct phylum of the domain Bacteria, and represent a fascinating group due to their unusual features such as intracellular compartmentalization and lack of peptidoglycan in their cell walls. The phylum Planctomycetes was described already in 1924, but still the diversity of this phylum represents an enigma and unexploited resource. In this study the diversity of the phylum Planctomycetes in low temperature iron-hydroxide deposits at the Mohns Ridge, a part of the Arctic Mid Ocean Ridge (AMOR), was characterised by descriptive analysis of 16S rRNA gene sequences in combination with isolation of Planctomycetes strains. The 16S rRNA gene sequences were affiliated with three order within the phylum Planctomycetes namely the (i)Planctomycetales, (ii) “Candidatus Brocadiales” and (iii) Phycisphaerae in addition to sequences affiliating to hitherto unknown Planctomycetes. The majority of the sequences were affiliated with the CCM11a group (Phycisphaerae), and with the Pir4 group (Planctomycetaceae). Two strains from the order Planctomycetales were isolated. One strain (Plm2) showed high similarity to the previously isolated Planctomyces maris (99 % 16S rRNA sequence identity). The other strain (Pr1d) belonged to the Pir4 group, and showed highest identity with Rhodopirellula baltica (86 %), Blastopirellula marina (86 %) and Pirellula staleyi (85 %). Based on its physiological and biochemical properties, strain Pr1dT is considered to represent a new genus of the order Planctomycetales. We propose to classify the novel planctomycete in a new genus and species, Bythoypirellula goksoyri gen. nov., sp. nov., the type strain being Pr1dT.
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RESEARCH ARTICLE Open Access
2013Co-Authors: Mia M Bengtsson, Lise OvreasAbstract:Background: Bacteria belonging to Planctomycetes display several unique morphological and genetic features and are found in a wide variety of habitats on earth. Their ecological roles in these habitats are still poorly understood. Planctomycetes have previously been detected throughout the year on surfaces of the kelp Laminaria hyperborea from southwestern Norway. We aimed to make a detailed investigation of the abundance and phylogenetic diversity of Planctomycetes inhabiting these kelp surfaces. Results: Planctomycetes accounted for 51-53 % of the bacterial biofilm cells in July and September and 24 % in February according to fluorescence in situ hybridization (FISH) results. Several separate Planctomycetes lineages within Pirellulae, Planctomyces and OM190 were represented in 16S rRNA gene clone libraries and the most abundant clones belonged to yet uncultured lineages. In contrast to the abundance, the diversity of the planctomycete populations increased from July to February and was probably influenced by the aging of the kelp tissue. One planctomycete strain that was closely related to Rhodopirellula baltica was isolated using selective cultivation techniques. Conclusions: Biofilms on surfaces of L. hyperborea display an even higher proportion of Planctomycetes compared to other investigated planctomycete-rich habitats such as open water, sandy sediments and peat bogs. Th
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Planctomycetes dominate biofilms on surfaces of the kelp laminaria hyperborea
BMC Microbiology, 2010Co-Authors: Mia M Bengtsson, Lise OvreasAbstract:Bacteria belonging to Planctomycetes display several unique morphological and genetic features and are found in a wide variety of habitats on earth. Their ecological roles in these habitats are still poorly understood. Planctomycetes have previously been detected throughout the year on surfaces of the kelp Laminaria hyperborea from southwestern Norway. We aimed to make a detailed investigation of the abundance and phylogenetic diversity of Planctomycetes inhabiting these kelp surfaces. Planctomycetes accounted for 51-53% of the bacterial biofilm cells in July and September and 24% in February according to fluorescence in situ hybridization (FISH) results. Several separate Planctomycetes lineages within Pirellulae, Planctomyces and OM190 were represented in 16S rRNA gene clone libraries and the most abundant clones belonged to yet uncultured lineages. In contrast to the abundance, the diversity of the planctomycete populations increased from July to February and was probably influenced by the aging of the kelp tissue. One planctomycete strain that was closely related to Rhodopirellula baltica was isolated using selective cultivation techniques. Biofilms on surfaces of L. hyperborea display an even higher proportion of Planctomycetes compared to other investigated planctomycete-rich habitats such as open water, sandy sediments and peat bogs. The findings agree well with the hypothesis of the role of Planctomycetes as degraders of sulfated polymeric carbon in the marine environment as kelps produce such substances. In addition, the abundant planctomycete populations on kelp surfaces and in association with other eukaryotes suggest that coexistence with eukaryotes may be a key feature of many planctomycete lifestyles.
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Planctomycetes dominate biofilms on surfaces of the kelp laminaria hyperborea
BMC Microbiology, 2010Co-Authors: Mia M Bengtsson, Lise OvreasAbstract:Background Bacteria belonging to Planctomycetes display several unique morphological and genetic features and are found in a wide variety of habitats on earth. Their ecological roles in these habitats are still poorly understood. Planctomycetes have previously been detected throughout the year on surfaces of the kelp Laminaria hyperborea from southwestern Norway. We aimed to make a detailed investigation of the abundance and phylogenetic diversity of Planctomycetes inhabiting these kelp surfaces.
