Publications by authors named "Bruno Huettel"

69 Publications

The temperature-regulated DEAD-box RNA helicase CrhR interactome: Autoregulation and photosynthesis-related transcripts.

J Exp Bot 2021 Sep 9. Epub 2021 Sep 9.

Faculty of Biology, University of Freiburg, Schänzlestr., Freiburg, Germany.

RNA helicases play crucial functions in RNA biology. In plants, RNA helicases are encoded by large gene families, performing roles in abiotic stress responses, development, the post-transcriptional regulation of gene expression as well as house-keeping functions. Several of these RNA helicases are targeted to the organelles, mitochondria and chloroplasts. Cyanobacteria are the direct evolutionary ancestors of plant chloroplasts. The cyanobacterium Synechocystis 6803 encodes a single DEAD-box RNA helicase, CrhR, that is induced by a range of abiotic stresses, including low temperature. Though the ΔcrhR mutant exhibits a severe cold-sensitive phenotype, the physiological function(s) performed by CrhR have not been described. To identify transcripts interacting with CrhR, we performed RNA co-immunoprecipitation with extracts from a Synechocystis crhR deletion mutant expressing the FLAG-tagged native CrhR or a K57A mutated version with an anticipated enhanced RNA binding. The composition of the interactome was strikingly biased towards photosynthesis-associated and redox-controlled transcripts. A transcript highly enriched in all experiments was the crhR mRNA, suggesting an auto-regulatory molecular mechanism. The identified interactome explains the described physiological role of CrhR in response to the redox poise of the photosynthetic electron transport chain and characterizes CrhR as an enzyme with a diverse range of transcripts as molecular targets.
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http://dx.doi.org/10.1093/jxb/erab416DOI Listing
September 2021

The salmon louse genome: Copepod features and parasitic adaptations.

Genomics 2021 Aug 14;113(6):3666-3680. Epub 2021 Aug 14.

Institute of Marine Research, Postboks 1870 Nordnes, 5817 Bergen, Norway; Sea Lice Research Centre. Department of Biological Sciences, University of Bergen, Thormøhlens Gate 53, 5006 Bergen, Norway. Electronic address:

Copepods encompass numerous ecological roles including parasites, detrivores and phytoplankton grazers. Nonetheless, copepod genome assemblies remain scarce. Lepeophtheirus salmonis is an economically and ecologically important ectoparasitic copepod found on salmonid fish. We present the 695.4 Mbp L. salmonis genome assembly containing ≈60% repetitive regions and 13,081 annotated protein-coding genes. The genome comprises 14 autosomes and a ZZ-ZW sex chromosome system. Assembly assessment identified 92.4% of the expected arthropod genes. Transcriptomics supported annotation and indicated a marked shift in gene expression after host attachment, including apparent downregulation of genes related to circadian rhythm coinciding with abandoning diurnal migration. The genome shows evolutionary signatures including loss of genes needed for peroxisome biogenesis, presence of numerous FNII domains, and an incomplete heme homeostasis pathway suggesting heme proteins to be obtained from the host. Despite repeated development of resistance against chemical treatments L. salmonis exhibits low numbers of many genes involved in detoxification.
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http://dx.doi.org/10.1016/j.ygeno.2021.08.002DOI Listing
August 2021

Microbial metagenome-assembled genomes of the Fram Strait from short and long read sequencing platforms.

PeerJ 2021 30;9:e11721. Epub 2021 Jun 30.

Department of Molecular Ecology, Max Planck Institute for Marine Microbiology, Bremen, Germany.

The impacts of climate change on the Arctic Ocean are manifesting throughout the ecosystem at an unprecedented rate. Of global importance are the impacts on heat and freshwater exchange between the Arctic and North Atlantic Oceans. An expanding Atlantic influence in the Arctic has accelerated sea-ice decline, weakened water column stability and supported the northward shift of temperate species. The only deep-water gateway connecting the Arctic and North Atlantic and thus, fundamental for these exchange processes is the Fram Strait. Previous research in this region is extensive, however, data on the ecology of microbial communities is limited, reflecting the wider bias towards temperate and tropical latitudes. Therefore, we present 14 metagenomes, 11 short-read from Illumina and three long-read from PacBio Sequel II, of the 0.2-3 µm fraction to help alleviate such biases and support future analyses on changing ecological patterns. Additionally, we provide 136 species-representative, manually refined metagenome-assembled genomes which can be used for comparative genomics analyses and addressing questions regarding functionality or distribution of taxa.
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http://dx.doi.org/10.7717/peerj.11721DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8254474PMC
June 2021

Plastome evolution in the Caesalpinia group (Leguminosae) and its application in phylogenomics and populations genetics.

Planta 2021 Jul 8;254(2):27. Epub 2021 Jul 8.

Laboratory of Plant Cytogenetics and Evolution, Department of Botany, Federal University of Pernambuco, Recife, Brazil.

Main Conclusion: The chloroplast genomes of Caesalpinia group species are structurally conserved, but sequence level variation is useful for both phylogenomic and population genetic analyses. Variation in chloroplast genomes (plastomes) has been an important source of information in plant biology. The Caesalpinia group has been used as a model in studies correlating ecological and genomic variables, yet its intergeneric and infrageneric relationships are not fully solved, despite densely sampled phylogenies including nuclear and plastid loci by Sanger sequencing. Here, we present the de novo assembly and characterization of plastomes from 13 species from the Caesalpinia group belonging to eight genera. A comparative analysis was carried out with 13 other plastomes previously available, totalizing 26 plastomes and representing 15 of the 26 known Caesalpinia group genera. All plastomes showed a conserved quadripartite structure and gene repertoire, except for the loss of four ndh genes in Erythrostemon gilliesii. Thirty polymorphic regions were identified for inter- or intrageneric analyses. The 26 aligned plastomes were used for phylogenetic reconstruction, revealing a well-resolved topology, and dividing the Caesalpinia group into two fully supported clades. Sixteen microsatellite (cpSSR) loci were selected from Cenostigma microphyllum for primer development and at least two were cross-amplified in different Leguminosae subfamilies by in vitro or in silico approaches. Four loci were used to assess the genetic diversity of C. microphyllum in the Brazilian Caatinga. Our results demonstrate the structural conservation of plastomes in the Caesalpinia group, offering insights into its systematics and evolution, and provides new genomic tools for future phylogenetic, population genetics, and phylogeographic studies.
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http://dx.doi.org/10.1007/s00425-021-03655-8DOI Listing
July 2021

Aiming off the target: recycling target capture sequencing reads for investigating repetitive DNA.

Ann Bot 2021 May 29. Epub 2021 May 29.

Laboratory of Plant Cytogenetics and Evolution, Department of Botany, Federal University of Pernambuco, Recife-PE, Brazil.

Background And Aims: With the advance of high-throughput sequencing (HTS), reduced-representation methods such as target capture sequencing (TCS) emerged as cost-efficient ways of gathering genomic information, particularly from coding regions. As the off-target reads from such sequencing are expected to be similar to genome skimming (GS), we assessed the quality of repeat characterization in plant genomes using this data.

Methods: Repeat composition obtained from TCS datasets of five Rhynchospora (Cyperaceae) species were compared with GS data from the same taxa. In addition, a FISH probe was designed based on the most abundant satellite found in the TCS dataset of Rhynchospora cephalotes. Finally, repeat-based phylogenies of the five Rhynchospora species were constructed based on the GS and TCS dataset and the topologies were compared with a gene-alignment based phylogenetic tree.

Key Results: All the major repetitive DNA families were identified in TCS, including repeats that showed abundances as low as 0.01% in the GS data. Rank correlation between GS and TCS repeat abundances were moderately high (r = 0.58-0.85), increasing after filtering out the targeted loci from the raw TCS reads (r = 0.66-0.92). Repeat data obtained by TCS was also reliable to develop a cytogenetic probe of a new variant of the holocentromeric satellite Tyba. Repeat-based phylogenies from TCS data were congruent with those obtained from GS data and the gene-alignment tree.

Conclusions: Our results show that off-target TCS reads can be recycled to identify repeats for cyto- and phylogenomic investigations. Given the growing availability of TCS reads, driven by global phylogenomic projects, our strategy represents a way to recycle genomic data and contribute to a better characterization of plant biodiversity.
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http://dx.doi.org/10.1093/aob/mcab063DOI Listing
May 2021

Genetic Diversity of Revealed by Multilocus Sequencing, and Identification of Populations Showing Genetic Isolation and Distinct Host Adaptation.

Front Plant Sci 2021 5;12:663027. Epub 2021 May 5.

Department of Biology, University of Kaiserslautern, Kaiserslautern, Germany.

is a world-wide occurring plant pathogen, causing pre- and post-harvest gray mold rot on a large number of fruit, vegetable, and flower crops. is closely related to , another broad host range species which often occurs in sympatry with , and to several host-specific species including and . populations have been shown to be genetically heterogeneous, and attempts have been made to correlate genetic markers to virulence and host adaptation. Here, we present the development of a multilocus sequence typing (MLST) scheme, with 10 genes selected for high variability and phylogenetic congruence, to evaluate the genetic diversity of , , and . Using PacBio-assisted simultaneous mass sequencing of PCR products, MLST analysis of about 100 strains from diverse geographical origins and years of isolation was performed, which resulted in high-resolution strain differentiation and robust species separation. Several strains formed an as yet unknown population, referred to as group B, which was well separated from all other strains. Furthermore, the gene cluster for biosynthesis of the phytotoxin botcinic acid was missing in B strains. strains from the monocot were found to form a genetically distinct population, and contained an intact gene cluster for production of the red pigment bikaverin, which is usually degenerated in . Remarkably, these strains were much more aggressive on than other strains, which is the first unequivocal example for host specialization in . Our data reveal new insights into the genetic diversity of and provide evidence for intraspecific differentiation and different degrees of host adaptation of this polyphagous necrotrophic pathogen.
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http://dx.doi.org/10.3389/fpls.2021.663027DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8131559PMC
May 2021

Two high-quality de novo genomes from single ethanol-preserved specimens of tiny metazoans (Collembola).

Gigascience 2021 May;10(5)

Max Planck Institute for Plant Breeding Research, Max Planck Genome-centre Cologne, Carl-von-Linné-Weg 10, 50829 Cologne, Germany.

Background: Genome sequencing of all known eukaryotes on Earth promises unprecedented advances in biological sciences and in biodiversity-related applied fields such as environmental management and natural product research. Advances in long-read DNA sequencing make it feasible to generate high-quality genomes for many non-genetic model species. However, long-read sequencing today relies on sizable quantities of high-quality, high molecular weight DNA, which is mostly obtained from fresh tissues. This is a challenge for biodiversity genomics of most metazoan species, which are tiny and need to be preserved immediately after collection. Here we present de novo genomes of 2 species of submillimeter Collembola. For each, we prepared the sequencing library from high molecular weight DNA extracted from a single specimen and using a novel ultra-low input protocol from Pacific Biosciences. This protocol requires a DNA input of only 5 ng, permitted by a whole-genome amplification step.

Results: The 2 assembled genomes have N50 values >5.5 and 8.5 Mb, respectively, and both contain ∼96% of BUSCO genes. Thus, they are highly contiguous and complete. The genomes are supported by an integrative taxonomy approach including placement in a genome-based phylogeny of Collembola and designation of a neotype for 1 of the species. Higher heterozygosity values are recorded in the more mobile species. Both species are devoid of the biosynthetic pathway for β-lactam antibiotics known in several Collembola, confirming the tight correlation of antibiotic synthesis with the species way of life.

Conclusions: It is now possible to generate high-quality genomes from single specimens of minute, field-preserved metazoans, exceeding the minimum contig N50 (1 Mb) required by the Earth BioGenome Project.
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http://dx.doi.org/10.1093/gigascience/giab035DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8138834PMC
May 2021

Anaerobic endosymbiont generates energy for ciliate host by denitrification.

Nature 2021 Mar 3;591(7850):445-450. Epub 2021 Mar 3.

Max Planck Institute for Marine Microbiology, Bremen, Germany.

Mitochondria are specialized eukaryotic organelles that have a dedicated function in oxygen respiration and energy production. They evolved about 2 billion years ago from a free-living bacterial ancestor (probably an alphaproteobacterium), in a process known as endosymbiosis. Many unicellular eukaryotes have since adapted to life in anoxic habitats and their mitochondria have undergone further reductive evolution. As a result, obligate anaerobic eukaryotes with mitochondrial remnants derive their energy mostly from fermentation. Here we describe 'Candidatus Azoamicus ciliaticola', which is an obligate endosymbiont of an anaerobic ciliate and has a dedicated role in respiration and providing energy for its eukaryotic host. 'Candidatus A. ciliaticola' contains a highly reduced 0.29-Mb genome that encodes core genes for central information processing, the electron transport chain, a truncated tricarboxylic acid cycle, ATP generation and iron-sulfur cluster biosynthesis. The genome encodes a respiratory denitrification pathway instead of aerobic terminal oxidases, which enables its host to breathe nitrate instead of oxygen. 'Candidatus A. ciliaticola' and its ciliate host represent an example of a symbiosis that is based on the transfer of energy in the form of ATP, rather than nutrition. This discovery raises the possibility that eukaryotes with mitochondrial remnants may secondarily acquire energy-providing endosymbionts to complement or replace functions of their mitochondria.
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http://dx.doi.org/10.1038/s41586-021-03297-6DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7969357PMC
March 2021

Gamete binning: chromosome-level and haplotype-resolved genome assembly enabled by high-throughput single-cell sequencing of gamete genomes.

Genome Biol 2020 12 29;21(1):306. Epub 2020 Dec 29.

Department of Chromosome Biology, Max Planck Institute for Plant Breeding Research, Carl-von-Linné-Weg 10, 50829, Cologne, Germany.

Generating chromosome-level, haplotype-resolved assemblies of heterozygous genomes remains challenging. To address this, we developed gamete binning, a method based on single-cell sequencing of haploid gametes enabling separation of the whole-genome sequencing reads into haplotype-specific reads sets. After assembling the reads of each haplotype, the contigs are scaffolded to chromosome level using a genetic map derived from the gametes. We assemble the two genomes of a diploid apricot tree based on whole-genome sequencing of 445 individual pollen grains. The two haplotype assemblies (N50: 25.5 and 25.8 Mb) feature a haplotyping precision of greater than 99% and are accurately scaffolded to chromosome-level.
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http://dx.doi.org/10.1186/s13059-020-02235-5DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7771071PMC
December 2020

Utilizing PacBio Iso-Seq for Novel Transcript and Gene Discovery of Abiotic Stress Responses in L.

Int J Mol Sci 2020 Oct 31;21(21). Epub 2020 Oct 31.

Max Planck Institute of Molecular Plant Physiology, Am Mühlenberg 1, 14476 Potsdam, Germany.

The wide natural variation present in rice is an important source of genes to facilitate stress tolerance breeding. However, identification of candidate genes from RNA-Seq studies is hampered by the lack of high-quality genome assemblies for the most stress tolerant cultivars. A more targeted solution is the reconstruction of transcriptomes to provide templates to map RNA-seq reads. Here, we sequenced transcriptomes of ten rice cultivars of three subspecies on the PacBio Sequel platform. RNA was isolated from different organs of plants grown under control and abiotic stress conditions in different environments. Reconstructed de novo reference transcriptomes resulted in 37,500 to 54,600 plant-specific high-quality isoforms per cultivar. Isoforms were collapsed to reduce sequence redundancy and evaluated, e.g., for protein completeness (BUSCO). About 40% of all identified transcripts were novel isoforms compared to the Nipponbare reference transcriptome. For the drought/heat tolerant cultivar N22, 56 differentially expressed genes in developing seeds were identified at combined heat and drought in the field. The newly generated rice transcriptomes are useful to identify candidate genes for stress tolerance breeding not present in the reference transcriptomes/genomes. In addition, our approach provides a cost-effective alternative to genome sequencing for identification of candidate genes in highly stress tolerant genotypes.
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http://dx.doi.org/10.3390/ijms21218148DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7663775PMC
October 2020

Draft Genome Sequence of " Phytoplasma pruni" (X-Disease Group, Subgroup 16SrIII-B) Strain ChTDIII from Argentina.

Microbiol Resour Announc 2020 Sep 17;9(38). Epub 2020 Sep 17.

Instituto Nacional de Tecnología Agropecuaria, Centro de Investigaciones Agropecuarias, Instituto de Patología Vegetal, Córdoba, Argentina

Herein, we report the draft genome sequence of " Phytoplasma pruni" strain ChTDIII (subgroup 16SrIII-B). The final assembly consists of 790,517 nucleotides organized in 67 contigs (minimal size, 1 kb), with a G+C content of 29.4% and encoding 672 proteins.
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http://dx.doi.org/10.1128/MRA.00792-20DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7498431PMC
September 2020

Identification of a Novel LysR-Type Transcriptional Regulator in Staphylococcus aureus That Is Crucial for Secondary Tissue Colonization during Metastatic Bloodstream Infection.

mBio 2020 08 25;11(4). Epub 2020 Aug 25.

Chair of Microbiology, Biocenter, University of Würzburg, Würzburg, Germany.

is a common cause of bacteremia that can lead to severe complications once the bacteria exit the bloodstream and establish infection in secondary organs. Despite its clinical relevance, little is known about the bacterial factors facilitating the development of these metastatic infections. Here, we used an transposon mutant library coupled to transposon insertion sequencing (Tn-Seq) to identify genes that are critical for efficient bacterial colonization of secondary organs in a murine model of metastatic bloodstream infection. Our transposon screen identified a LysR-type transcriptional regulator (LTTR), which was required for efficient colonization of secondary organs such as the kidneys in infected mice. The critical role of LTTR in secondary organ colonization was confirmed using an isogenic mutant deficient in the expression of LTTR. To identify the set of genes controlled by LTTR, we used an strain carrying the LTTR gene in an inducible expression plasmid. Gene expression analysis upon induction of LTTR showed increased transcription of genes involved in branched-chain amino acid biosynthesis, a methionine sulfoxide reductase, and a copper transporter as well as decreased transcription of genes coding for urease and components of pyrimidine nucleotides. Furthermore, we show that transcription of LTTR is repressed by glucose, is induced under microaerobic conditions, and required trace amounts of copper ions. Our data thus pinpoints LTTR as an important element that enables a rapid adaptation of to the changing host microenvironment. is an important pathogen that can disseminate via the bloodstream and establish metastatic infections in distant organs. To achieve a better understanding of the bacterial factors facilitating the development of these metastatic infections, we used in this study a transposon mutant library in a murine model of intravenous infection, where bacteria first colonize the liver as the primary infection site and subsequently progress to secondary sites such as the kidney and bones. We identified a novel LysR-type transcriptional regulator (LTTR), which was specifically required by for efficient colonization of secondary organs. We also determined the transcriptional activation as well as the regulon of LTTR, which suggests that this regulator is involved in the metabolic adaptation of to the host microenvironment found in secondary infection sites.
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http://dx.doi.org/10.1128/mBio.01646-20DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7448277PMC
August 2020

Genome Sequences of Both Organelles of the Grapevine Rootstock Cultivar 'Börner'.

Microbiol Resour Announc 2020 Apr 9;9(15). Epub 2020 Apr 9.

Bielefeld University, Chair of Genetics and Genomics of Plants, Faculty of Biology & Center for Biotechnology (CeBiTec), Bielefeld, Germany

Genomic long reads of the interspecific grapevine rootstock cultivar 'Börner' ( GM183 × Arnold) were used to assemble its chloroplast and mitochondrion genome sequences. We annotated 133 chloroplast and 172 mitochondrial genes, including the RNA editing sites. The organelle genomes in 'Börner' were maternally inherited from .
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http://dx.doi.org/10.1128/MRA.01471-19DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7380517PMC
April 2020

The sugar transporter SWEET10 acts downstream of FLOWERING LOCUS T during floral transition of Arabidopsis thaliana.

BMC Plant Biol 2020 Feb 3;20(1):53. Epub 2020 Feb 3.

Max Planck Institute for Plant Breeding Research, Carl-von-Linne-Weg 10, 50829, Köln, Germany.

Background: Floral transition initiates reproductive development of plants and occurs in response to environmental and endogenous signals. In Arabidopsis thaliana, this process is accelerated by several environmental cues, including exposure to long days. The photoperiod-dependent promotion of flowering involves the transcriptional induction of FLOWERING LOCUS T (FT) in the phloem of the leaf. FT encodes a mobile protein that is transported from the leaves to the shoot apical meristem, where it forms part of a regulatory complex that induces flowering. Whether FT also has biological functions in leaves of wild-type plants remains unclear.

Results: In order to address this issue, we first studied the leaf transcriptomic changes associated with FT overexpression in the companion cells of the phloem. We found that FT induces the transcription of SWEET10, which encodes a bidirectional sucrose transporter, specifically in the leaf veins. Moreover, SWEET10 is transcriptionally activated by long photoperiods, and this activation depends on FT and one of its earliest target genes SUPPRESSOR OF CONSTANS OVEREXPRESSION 1 (SOC1). The ectopic expression of SWEET10 causes early flowering and leads to higher levels of transcription of flowering-time related genes in the shoot apex.

Conclusions: Collectively, our results suggest that the FT-signaling pathway activates the transcription of a sucrose uptake/efflux carrier during floral transition, indicating that it alters the metabolism of flowering plants as well as reprogramming the transcription of floral regulators in the shoot meristem.
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http://dx.doi.org/10.1186/s12870-020-2266-0DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6998834PMC
February 2020

Evolutionary convergence or homology? Comparative cytogenomics of Caesalpinia group species (Leguminosae) reveals diversification in the pericentromeric heterochromatic composition.

Planta 2019 Dec 6;250(6):2173-2186. Epub 2019 Nov 6.

Laboratory of Plant Cytogenetics and Evolution, Department of Botany, Federal University of Pernambuco, Rua Nelson Chaves S/N, Cidade Universitária, Recife, PE, 50670-420, Brazil.

Main Conclusion: We demonstrated by cytogenomic analysis that the proximal heterochromatin of the Northeast Brazilian species of Caesalpinia group is enriched with phylogenetically conserved Ty3/Gypsy-Tekay RT, but diverge in the presence of Ty3/Gypsy-Athila RT and satDNA. The Caesalpinia Group includes 225 species and 27 monophyletic genera of which four occur in Northeastern Brazil: Erythrostemon (1 sp.), Cenostigma (7 spp.), Libidibia (1 sp.), and Paubrasilia (1 sp.). The last three genera are placed in different clades in the Caesalpinia Group phylogeny, and yet they are characterized by having a numerically stable karyotype 2n = 24 (16 M+8A) and GC-rich heterochromatic bands (chromomycin A positive/CMA bands) in the proximal chromosome regions. To characterize the composition of their heterochromatin and test for the homology of these chromosomal regions, genomic DNA was extracted from Cenostigma microphyllum, Libidibia ferrea, and Paubrasilia echinata, and sequenced at low coverage using the Illumina platform. The genomic repetitive fractions were characterized using a Galaxy/RepeatExplorer-Elixir platform. The most abundant elements of each genome were chromosomally located by fluorescent in situ hybridization (FISH) and compared to the CMA heterochromatin distribution. The repetitive fraction of the genomes of C. microphyllum, L. ferrea, and P. echinata were estimated to be 41.70%, 38.44%, and 72.51%, respectively. Ty3/Gypsy retrotransposons (RT), specifically the Tekay lineage, were the most abundant repeats in each of the three genomes. FISH mapping revealed species-specific patterns for the Tekay elements in the proximal regions of the chromosomes, co-localized with CMA bands. Other species-specific patterns were observed, e.g., for the Ty3/Gypsy RT Athila elements which were found in all the proximal heterochromatin of L. ferrea or restricted to the acrocentric chromosomes of C. microphyllum. This Athila labeling co-localized with satellite DNAs (satDNAs). Although the Caesalpinia Group diverged around 55 Mya, our results suggest an ancestral colonization of Tekay RT in the proximal heterochromatin. Thus, the present-day composition of the pericentromeric heterochromatin in these Northeast Brazilian species is a combination of the maintenance of an ancestral Tekay distribution with a species-specific accumulation of other repeats.
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http://dx.doi.org/10.1007/s00425-019-03287-zDOI Listing
December 2019

Interplay and Targetome of the Two Conserved Cyanobacterial sRNAs Yfr1 and Yfr2 in Prochlorococcus MED4.

Sci Rep 2019 10 4;9(1):14331. Epub 2019 Oct 4.

University of Freiburg, Faculty of Biology, D-79104, Freiburg, Germany.

The sRNA Yfr1 and members of the Yfr2 sRNA family are almost universally present within cyanobacteria. The conserved motifs of these sRNAs are nearly complementary to each other, suggesting their ability to participate in crosstalk. The conserved motif of Yfr1 is shared by members of the Yfr10 sRNA family, members of which are otherwise less conserved in sequence, structure, and synteny compared to Yfr1. The different structural properties enable the discrimination of unique targets of Yfr1 and Yfr10. Unlike most studied regulatory sRNAs, Yfr1 gene expression only slightly changes under the tested stress conditions and is present at high levels at all times. In contrast, cellular levels of Yfr10 increase during the course of acclimation to darkness, and levels of Yfr2 increase when cells are shifted to high light or nitrogen limitation conditions. In this study, we investigated the targetomes of Yfr2, Yfr1, and Yfr10 in Prochlorococcus MED4, establishing CRAFD-Seq as a new method for identifying direct targets of these sRNAs that is applicable to all bacteria, including those that are not amenable to genetic modification. The results suggest that these sRNAs are integrated within a regulatory network of unprecedented complexity in the adjustment of carbon and nitrogen-related primary metabolism.
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http://dx.doi.org/10.1038/s41598-019-49881-9DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6778093PMC
October 2019

Linked-read sequencing of gametes allows efficient genome-wide analysis of meiotic recombination.

Nat Commun 2019 09 20;10(1):4310. Epub 2019 Sep 20.

Department of Chromosome Biology, Max Planck Institute for Plant Breeding Research, Carl-von-Linné-Weg 10, 50829, Cologne, Germany.

Meiotic crossovers (COs) ensure proper chromosome segregation and redistribute the genetic variation that is transmitted to the next generation. Large populations and the demand for genome-wide, fine-scale resolution challenge existing methods for CO identification. Taking advantage of linked-read sequencing, we develop a highly efficient method for genome-wide identification of COs at kilobase resolution in pooled recombinants. We first test this method using a pool of Arabidopsis F recombinants, and recapitulate results obtained from the same plants using individual whole-genome sequencing. By applying this method to a pool of pollen DNA from an F plant, we establish a highly accurate CO landscape without generating or sequencing a single recombinant plant. The simplicity of this approach enables the simultaneous generation and analysis of multiple CO landscapes, accelerating the pace at which mechanisms for the regulation of recombination can be elucidated through efficient comparisons of genotypic and environmental effects on recombination.
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http://dx.doi.org/10.1038/s41467-019-12209-2DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6754367PMC
September 2019

Sulfur-Oxidizing Symbionts without Canonical Genes for Autotrophic CO Fixation.

mBio 2019 06 25;10(3). Epub 2019 Jun 25.

Max Planck Institute for Marine Microbiology, Bremen, Germany.

Since the discovery of symbioses between sulfur-oxidizing (thiotrophic) bacteria and invertebrates at hydrothermal vents over 40 years ago, it has been assumed that autotrophic fixation of CO by the symbionts drives these nutritional associations. In this study, we investigated " Kentron," the clade of symbionts hosted by , a diverse genus of ciliates which are found in marine coastal sediments around the world. Despite being the main food source for their hosts, Kentron bacteria lack the key canonical genes for any of the known pathways for autotrophic carbon fixation and have a carbon stable isotope fingerprint that is unlike other thiotrophic symbionts from similar habitats. Our genomic and transcriptomic analyses instead found metabolic features consistent with growth on organic carbon, especially organic and amino acids, for which they have abundant uptake transporters. All known thiotrophic symbionts have converged on using reduced sulfur to gain energy lithotrophically, but they are diverse in their carbon sources. Some clades are obligate autotrophs, while many are mixotrophs that can supplement autotrophic carbon fixation with heterotrophic capabilities similar to those in Kentron. Here we show that Kentron bacteria are the only thiotrophic symbionts that appear to be entirely heterotrophic, unlike all other thiotrophic symbionts studied to date, which possess either the Calvin-Benson-Bassham or the reverse tricarboxylic acid cycle for autotrophy. Many animals and protists depend on symbiotic sulfur-oxidizing bacteria as their main food source. These bacteria use energy from oxidizing inorganic sulfur compounds to make biomass autotrophically from CO, serving as primary producers for their hosts. Here we describe a clade of nonautotrophic sulfur-oxidizing symbionts, " Kentron," associated with marine ciliates. They lack genes for known autotrophic pathways and have a carbon stable isotope fingerprint heavier than other symbionts from similar habitats. Instead, they have the potential to oxidize sulfur to fuel the uptake of organic compounds for heterotrophic growth, a metabolic mode called chemolithoheterotrophy that is not found in other symbioses. Although several symbionts have heterotrophic features to supplement primary production, in Kentron they appear to supplant it entirely.
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http://dx.doi.org/10.1128/mBio.01112-19DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6593406PMC
June 2019

A chromosome-level sequence assembly reveals the structure of the Arabidopsis thaliana Nd-1 genome and its gene set.

PLoS One 2019 21;14(5):e0216233. Epub 2019 May 21.

Bielefeld University, Faculty of Biology & Center for Biotechnology, Bielefeld, Germany.

In addition to the BAC-based reference sequence of the accession Columbia-0 from the year 2000, several short read assemblies of THE plant model organism Arabidopsis thaliana were published during the last years. Also, a SMRT-based assembly of Landsberg erecta has been generated that identified translocation and inversion polymorphisms between two genotypes of the species. Here we provide a chromosome-arm level assembly of the A. thaliana accession Niederzenz-1 (AthNd-1_v2c) based on SMRT sequencing data. The best assembly comprises 69 nucleome sequences and displays a contig length of up to 16 Mbp. Compared to an earlier Illumina short read-based NGS assembly (AthNd-1_v1), a 75 fold increase in contiguity was observed for AthNd-1_v2c. To assign contig locations independent from the Col-0 gold standard reference sequence, we used genetic anchoring to generate a de novo assembly. In addition, we assembled the chondrome and plastome sequences. Detailed analyses of AthNd-1_v2c allowed reliable identification of large genomic rearrangements between A. thaliana accessions contributing to differences in the gene sets that distinguish the genotypes. One of the differences detected identified a gene that is lacking from the Col-0 gold standard sequence. This de novo assembly extends the known proportion of the A. thaliana pan-genome.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0216233PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6529160PMC
January 2020

Development of ten microsatellite markers for Alibertia edulis (Rubiaceae), a Brazilian savanna tree species.

Mol Biol Rep 2019 Aug 30;46(4):4593-4597. Epub 2019 Apr 30.

Laboratory of Plant Cytogenetics and Evolution, Department of Botany, Centre of Biosciences, Federal University of Pernambuco, R. Prof. Moraes Rego, s/n, CDU, Recife, PE, 50670-420, Brazil.

Ten microsatellite markers were developed using next-generation sequencing data for Alibertia edulis (Rubiaceae), a widely distributed species typical of Cerrado (Brazilian savanna) vegetation. The markers were polymorphic in the two populations analyzed. The numbers of alleles, and observed (H) and expected (H) heterozygosities per polymorphic locus ranged from 2 to 11, 0.091 to 1.0, and 0.100 to 0.937 respectively. The SSR loci demonstrated moderate to high polymorphism values in both populations analyzed, with PIC values ranging from 0.26 to 0.91, and total allele numbers ranging from three to 16. The inbreeding coefficient values were generally higher in the Piauí population (ranging from - 0.593 to 0.762) than in the Mato Grosso population (ranging from - 1 to 0.575). The differences observed between those disjunct populations suggest they harbor different alleles, which has implications for Cerrado conservation strategies. Those loci will be useful for population studies of A. edulis.
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http://dx.doi.org/10.1007/s11033-019-04819-2DOI Listing
August 2019

Development and characterization of eleven microsatellite loci for the tropical understory tree Paypayrola blanchetiana Tul. (Violaceae).

Mol Biol Rep 2019 Apr 28;46(2):2529-2532. Epub 2019 Jan 28.

Laboratory of Plant Cytogenetics and Evolution, Department of Botany, Center of Biosciences, Federal University of Pernambuco, R. Prof. Moraes Rego, s/n, CDU, Recife, PE, 50670-420, Brazil.

Microsatellites markers were developed for Paypayrola blanchetiana (Violaceae), a near-dispersing forest tree forming aggregated populations, to investigate genetic diversity and gene flow among subpopulations in a fragmented environment. Next generation sequencing (Illumina platform) was used to develop ten nuclear microsatellite loci and one plastid microsatellite locus that amplify in P. blanchetiana. Polymorphism was tested in two subpopulations separated by a distance of approximately 11 km. The identified loci contained between two and five alleles per locus. Observed heterozygosity ranged between 0.063 and 0.563 in both subpopulations, while expected heterozygosity ranged from 0.063 to 0.567 in the first, and 0.063-0.627 in the second subpopulation. The microsatellites are among the first in the family Violaceae and will be useful for population genetic studies in this species. Amplification was successful in one further Paypayrola species from Amazonia, which suggest a wider usefulness of the present markers.
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http://dx.doi.org/10.1007/s11033-019-04622-zDOI Listing
April 2019

Global impacts of chromosomal imbalance on gene expression in and other taxa.

Proc Natl Acad Sci U S A 2018 11 14;115(48):E11321-E11330. Epub 2018 Nov 14.

Division of Biological Sciences, University of Missouri, Columbia, MO 65211;

Changes in dosage of part of the genome (aneuploidy) have long been known to produce much more severe phenotypic consequences than changes in the number of whole genomes (ploidy). To examine the basis of these differences, global gene expression in mature leaf tissue for all five trisomies and in diploids, triploids, and tetraploids of was studied. The trisomies displayed a greater spread of expression modulation than the ploidy series. In general, expression of genes on the varied chromosome ranged from compensation to dosage effect, whereas genes from the remainder of the genome ranged from no effect to reduced expression approaching the inverse level of chromosomal imbalance (2/3). Genome-wide DNA methylation was examined in each genotype and found to shift most prominently with trisomy 4 but otherwise exhibited little change, indicating that genetic imbalance is generally mechanistically unrelated to DNA methylation. Independent analysis of gene functional classes demonstrated that ribosomal, proteasomal, and gene body methylated genes were less modulated compared with all classes of genes, whereas transcription factors, signal transduction components, and organelle-targeted protein genes were more tightly inversely affected. Comparing transcription factors and their targets in the trisomies and in expression networks revealed considerable discordance, illustrating that altered regulatory stoichiometry is a major contributor to genetic imbalance. Reanalysis of published data on gene expression in disomic yeast and trisomic mouse cells detected similar stoichiometric effects across broad phylogenetic taxa, and indicated that these effects reflect normal gene regulatory processes.
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http://dx.doi.org/10.1073/pnas.1807796115DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6275517PMC
November 2018

Development of 15 nuclear microsatellite markers in (Pitcairnioideae; Bromeliaceae) using 454 pyrosequencing.

Appl Plant Sci 2018 Apr 8;6(4):e1147. Epub 2018 May 8.

Biological Sciences Pantanal Campus/Federal University of Mato Grosso do Sul State C.P. 252 79304-902 Corumbá Brazil.

Premise Of The Study: Microsatellite markers were developed in (Bromeliaceae) to investigate species and subspecies boundaries within the genus and the genetic diversity of natural populations.

Methods And Results: We used 454 pyrosequencing to isolate 835 microsatellite loci in . Of 64 loci selected for primer design, 15 were polymorphic among 23 individuals of and 76 individuals of the heterologous subspecies subsp. and subsp. . Twelve and 13 of these loci were also polymorphic in one population each of and , respectively. Numbers of alleles per locus varied from two to 14 in , two to 12 in , one to nine in , and one to 10 in . STRUCTURE analyses clearly separated the taxa from each other.

Conclusions: The 15 new microsatellite markers are promising tools for studying population genetics in species.
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http://dx.doi.org/10.1002/aps3.1147DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5947610PMC
April 2018

Aberrant imprinting may underlie evolution of parthenogenesis.

Sci Rep 2018 Jul 13;8(1):10626. Epub 2018 Jul 13.

University of Heidelberg, Centre for Organismal Studies, Laboratory of Germline Genetics & Evo-Devo, Heidelberg, Germany.

Genomic imprinting confers parent-of-origin-specific gene expression, thus non-equivalent and complementary function of parental genomes. As a consequence, genomic imprinting poses an epigenetic barrier to parthenogenesis in sexual organisms. We report aberrant imprinting in Boechera, a genus in which apomicts evolved from sexuals multiple times. Maternal activation of a MADS-box gene, a homolog of which is imprinted and paternally expressed in the sexual relative Arabidopsis, is accompanied by locus-specific DNA methylation changes in apomicts where parental imprinting seems to be relaxed.
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http://dx.doi.org/10.1038/s41598-018-27863-7DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6045609PMC
July 2018

Fern genomes elucidate land plant evolution and cyanobacterial symbioses.

Nat Plants 2018 07 2;4(7):460-472. Epub 2018 Jul 2.

University Herbarium and Department of Integrative Biology, University of California, Berkeley, CA, USA.

Ferns are the closest sister group to all seed plants, yet little is known about their genomes other than that they are generally colossal. Here, we report on the genomes of Azolla filiculoides and Salvinia cucullata (Salviniales) and present evidence for episodic whole-genome duplication in ferns-one at the base of 'core leptosporangiates' and one specific to Azolla. One fern-specific gene that we identified, recently shown to confer high insect resistance, seems to have been derived from bacteria through horizontal gene transfer. Azolla coexists in a unique symbiosis with N-fixing cyanobacteria, and we demonstrate a clear pattern of cospeciation between the two partners. Furthermore, the Azolla genome lacks genes that are common to arbuscular mycorrhizal and root nodule symbioses, and we identify several putative transporter genes specific to Azolla-cyanobacterial symbiosis. These genomic resources will help in exploring the biotechnological potential of Azolla and address fundamental questions in the evolution of plant life.
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http://dx.doi.org/10.1038/s41477-018-0188-8DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6786969PMC
July 2018

Single molecule real time sequencing in ADTKD-MUC1 allows complete assembly of the VNTR and exact positioning of causative mutations.

Sci Rep 2018 03 8;8(1):4170. Epub 2018 Mar 8.

Institute of Human Genetics, University Hospital of Cologne, Cologne, Germany.

Recently, the Mucin-1 (MUC1) gene has been identified as a causal gene of autosomal dominant tubulointerstitial kidney disease (ADTKD). Most causative mutations are buried within a GC-rich 60 basepair variable number of tandem repeat (VNTR), which escapes identification by massive parallel sequencing methods due to the complexity of the VNTR. We established long read single molecule real time sequencing (SMRT) targeted to the MUC1-VNTR as an alternative strategy to the snapshot assay. Our approach allows complete VNTR assembly, thereby enabling the detection of all variants residing within the VNTR and simultaneous determination of VNTR length. We present high resolution data on the VNTR architecture for a cohort of snapshot positive (n = 9) and negative (n = 7) ADTKD families. By SMRT sequencing we could confirm the diagnosis in all previously tested cases, reconstruct both VNTR alleles and determine the exact position of the causative variant in eight of nine families. This study demonstrates that precise positioning of the causative mutation(s) and identification of other coding and noncoding sequence variants in ADTKD-MUC1 is feasible. SMRT sequencing could provide a powerful tool to uncover potential factors encoded within the VNTR that associate with intra- and interfamilial phenotype variability of MUC1 related kidney disease.
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http://dx.doi.org/10.1038/s41598-018-22428-0DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5843638PMC
March 2018

Identification of the DNA methyltransferases establishing the methylome of the cyanobacterium Synechocystis sp. PCC 6803.

DNA Res 2018 Aug;25(4):343-352

Faculty of Biology, University of Freiburg, Freiburg, Germany.

DNA methylation in bacteria is important for defense against foreign DNA, but is also involved in DNA repair, replication, chromosome partitioning, and regulatory processes. Thus, characterization of the underlying DNA methyltransferases in genetically tractable bacteria is of paramount importance. Here, we characterized the methylome and orphan methyltransferases in the model cyanobacterium Synechocystis sp. PCC 6803. Single molecule real-time (SMRT) sequencing revealed four DNA methylation recognition sequences in addition to the previously known motif m5CGATCG, which is recognized by M.Ssp6803I. For three of the new recognition sequences, we identified the responsible methyltransferases. M.Ssp6803II, encoded by the sll0729 gene, modifies GGm4CC, M.Ssp6803III, encoded by slr1803, represents the cyanobacterial dam-like methyltransferase modifying Gm6ATC, and M.Ssp6803V, encoded by slr6095 on plasmid pSYSX, transfers methyl groups to the bipartite motif GGm6AN7TTGG/CCAm6AN7TCC. The remaining methylation recognition sequence GAm6AGGC is probably recognized by methyltransferase M.Ssp6803IV encoded by slr6050. M.Ssp6803III and M.Ssp6803IV were essential for the viability of Synechocystis, while the strains lacking M.Ssp6803I and M.Ssp6803V showed growth similar to the wild type. In contrast, growth was strongly diminished of the Δsll0729 mutant lacking M.Ssp6803II. These data provide the basis for systematic studies on the molecular mechanisms impacted by these methyltransferases.
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http://dx.doi.org/10.1093/dnares/dsy006DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6105098PMC
August 2018

Benefit from decline: the primary transcriptome of Alteromonas macleodii str. Te101 during Trichodesmium demise.

ISME J 2018 04 15;12(4):981-996. Epub 2018 Jan 15.

Faculty of Biology, University of Freiburg, Schänzlestr. 1, D-79104, Freiburg, Germany.

Interactions between co-existing microorganisms deeply affect the physiology of the involved organisms and, ultimately, the function of the ecosystem as a whole. Copiotrophic Alteromonas are marine gammaproteobacteria that thrive during the late stages of phytoplankton blooms in the marine environment and in laboratory co-cultures with cyanobacteria such as Trichodesmium. The response of this heterotroph to the sometimes rapid and transient changes in nutrient supply when the phototroph crashes is not well understood. Here, we isolated and sequenced the strain Alteromonas macleodii str. Te101 from a laboratory culture of Trichodesmium erythraeum IMS101, yielding a chromosome of 4.63 Mb and a single plasmid of 237 kb. Increasing salinities to ≥43 ppt inhibited the growth of Trichodesmium but stimulated growth of the associated Alteromonas. We characterized the transcriptomic responses of both microorganisms and identified the complement of active transcriptional start sites in Alteromonas at single-nucleotide resolution. In replicate cultures, a similar set of genes became activated in Alteromonas when growth rates of Trichodesmium declined and mortality was high. The parallel activation of fliA, rpoS and of flagellar assembly and growth-related genes indicated that Alteromonas might have increased cell motility, growth, and multiple biosynthetic activities. Genes with the highest expression in the data set were three small RNAs (Aln1a-c) that were identified as analogs of the small RNAs CsrB-C in E. coli or RsmX-Z in pathogenic bacteria. Together with the carbon storage protein A (CsrA) homolog Te101_05290, these RNAs likely control the expression of numerous genes in responding to changes in the environment.
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http://dx.doi.org/10.1038/s41396-017-0034-4DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5864184PMC
April 2018

Flowering Time Gene Variation in Species Shows Evolutionary Principles.

Front Plant Sci 2017 17;8:1742. Epub 2017 Oct 17.

Department of Plant Breeding, IFZ Research Centre for Biosystems, Land Use and Nutrition, Justus Liebig University, Giessen, Germany.

Flowering time genes have a strong influence on successful reproduction and life cycle adaptation. However, their regulation is highly complex and only well understood in diploid model systems. For crops with a polyploid background from the genus , data on flowering time gene variation are scarce, although indispensable for modern breeding techniques like marker-assisted breeding. We have deep-sequenced all paralogs of 35 flowering regulators using Sequence Capture followed by Illumina sequencing in two selected accessions of the vegetable species and , respectively. Using these data, we were able to call SNPs, InDels and copy number variations (CNVs) for genes from the total flowering time network including central flowering regulators, but also genes from the vernalisation pathway, the photoperiod pathway, temperature regulation, the circadian clock and the downstream effectors. Comparing the results to a complementary data set from the allotetraploid species , we detected rearrangements in which probably occurred early after the allopolyploidisation event. Those data are both a valuable resource for flowering time research in those vegetable species, as well as a contribution to speciation genetics.
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http://dx.doi.org/10.3389/fpls.2017.01742DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5651034PMC
October 2017

Is there foul play in the leaf pocket? The metagenome of floating fern Azolla reveals endophytes that do not fix N but may denitrify.

New Phytol 2018 Jan 30;217(1):453-466. Epub 2017 Oct 30.

Molecular Plant Physiology Department, Utrecht University, Padualaan 8, Utrecht, 3584CH, the Netherlands.

Dinitrogen fixation by Nostoc azollae residing in specialized leaf pockets supports prolific growth of the floating fern Azolla filiculoides. To evaluate contributions by further microorganisms, the A. filiculoides microbiome and nitrogen metabolism in bacteria persistently associated with Azolla ferns were characterized. A metagenomic approach was taken complemented by detection of N O released and nitrogen isotope determinations of fern biomass. Ribosomal RNA genes in sequenced DNA of natural ferns, their enriched leaf pockets and water filtrate from the surrounding ditch established that bacteria of A. filiculoides differed entirely from surrounding water and revealed species of the order Rhizobiales. Analyses of seven cultivated Azolla species confirmed persistent association with Rhizobiales. Two distinct nearly full-length Rhizobiales genomes were identified in leaf-pocket-enriched samples from ditch grown A. filiculoides. Their annotation revealed genes for denitrification but not N -fixation. N incorporation was active in ferns with N. azollae but not in ferns without. N O was not detectably released from surface-sterilized ferns with the Rhizobiales. N -fixing N. azollae, we conclude, dominated the microbiome of Azolla ferns. The persistent but less abundant heterotrophic Rhizobiales bacteria possibly contributed to lowering O levels in leaf pockets but did not release detectable amounts of the strong greenhouse gas N O.
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http://dx.doi.org/10.1111/nph.14843DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5901025PMC
January 2018
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