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Effects and Dynamics of Insertion Sequences in the Evolution of Cyanobacteria
Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences. (Plant physiology)
2015 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Cyanobacteria are globally widespread and ecologically highly significant photoautotrophic microorganisms, with diverse geno- and phenotypic characters unprecedented among prokaryotes. This phylum embraces representatives with an exclusive adaptability in highly specialized environments, from oligotrophic ocean waters to the interior of cells in symbiotic plants, the most extreme being the chloroplasts. Insertion sequences (ISs) are short (~1000 bp) mobile genetic elements prevalent in microbial genomes, potentially representing potent adaptive forces.

In this thesis, hypotheses tested that ISs play significant roles in both reductive and adaptive evolution in physiologically versatile cyanobacteria, using two model systems. First, the genome of an obligate plant (Azolla) symbiont, the cyanobacterium ‘Nostoc azollae 0708’, was sequenced, which led to the discovery of a highly ‘eroding’ genome (5,48 Mbp), loaded with ISs covering 14% of the genome, a situation likely caused by the relaxed selection pressure within the plant. The ISs were located in close proximity to the extremely numerous pseudogenes identified, although genes with key functions in a symbiotic context escaped IS mediated erosion (e.g. nitrogen fixation and differentiation genes). Some ISs were shown to have transposed short distances within the genome (‘local hoping’), and to be likely causative agents in pseudogene formation, and thus pivotal actors in the reductive evolution discovered.

To widen the scope of ISs further, additionally 66 phylogenetically diverse microorganisms with a variety of life styles (free-living, symbionts, pathogens) were examined in regards to ISs influence. The data verified their over-all importance in shaping microbial genomes.

Finally, natural microbial populations in the Baltic Sea, a semi-enclosed geologically young (~10,000 years) brackish water body offering steep gradients in salinity and nutrient loads, were examined using metatranscriptomics and metagenomics. A large proportion of the metagenome was devoted to ISs and most importantly a large fraction of the metatranscriptome consisted of IS transcripts (~1%), which may be suggestive of a high IS activity. These phenomena were most apparent in cyanobacteria in central parts of the Baltic Sea. The presence of an especially rich abundance of ISs in brackish waters was further substantiated by their low frequency (< 0.1%) in microbes of marine waters. Hence, ISs may facilitate both adaptations (short term) and adaptive evolution (long term) in microbes entering brackish water, otherwise unable to cross the distinct limnic-to-marine salinity-divide. Together, the data reveal high genomic loads of ISs in cyanobacteria subject to highly demanding conditions and stress the importance of locally migrating ISs (and pseudogenization) as important facilitators in adaptation and evolution, being a more rapid process than hitherto expected. The findings strongly support current theories stating a crucial role of ISs in shaping microbial genomes to render fitness.

Place, publisher, year, edition, pages
Stockholm: Department of Ecology, Environment and Plant Sciences, Stockholm University , 2015. , 56 p.
Keyword [en]
Cyanobacteria, Insertion Sequences, Evolution
National Category
Botany
Research subject
Plant Physiology
Identifiers
URN: urn:nbn:se:su:diva-117090ISBN: 978-91-7649-191-1 (print)OAI: oai:DiVA.org:su-117090DiVA: diva2:810177
Public defence
2015-06-10, Lecture Hall, Department of Ecology, Environment and Plant Sciences, Lilla Frescativägen 5, Stockholm, 10:00 (English)
Opponent
Supervisors
Note

At the time of the doctoral defense, the following paper was unpublished and had a status as follows: Paper 3: Manuscript.

Available from: 2015-05-19 Created: 2015-05-06 Last updated: 2015-12-02Bibliographically approved
List of papers
1. Genome Erosion in a Nitrogen-Fixing Vertically Transmitted Endosymbiotic Multicellular Cyanobacterium
Open this publication in new window or tab >>Genome Erosion in a Nitrogen-Fixing Vertically Transmitted Endosymbiotic Multicellular Cyanobacterium
Show others...
2010 (English)In: PLoS ONE, ISSN 1932-6203, E-ISSN 1932-6203, Vol. 5, no 7, e11486Article in journal (Refereed) Published
Abstract [en]

Background: An ancient cyanobacterial incorporation into a eukaryotic organism led to the evolution of plastids (chloroplasts) and subsequently to the origin of the plant kingdom. The underlying mechanism and the identities of the partners in this monophyletic event remain elusive.

Methodology/Principal Findings: To shed light on this evolutionary process, we sequenced the genome of a cyanobacterium residing extracellularly in an endosymbiosis with a plant, the water-fern Azolla filiculoides Lam. This symbiosis was selected as it has characters which make it unique among extant cyanobacterial plant symbioses: the cyanobacterium lacks autonomous growth and is vertically transmitted between plant generations. Our results reveal features of evolutionary significance. The genome is in an eroding state, evidenced by a large proportion of pseudogenes (31.2%) and a high frequency of transposable elements (,600) scattered throughout the genome. Pseudogenization is found in genes such as the replication initiator dnaA and DNA repair genes, considered essential to free-living cyanobacteria. For some functional categories of genes pseudogenes are more prevalent than functional genes. Loss of function is apparent even within the ‘core’ gene categories of bacteria, such as genes involved in glycolysis and nutrient uptake. In contrast, serving as a critical source of nitrogen for the host, genes related to metabolic processes such as cell differentiation and nitrogen-fixation are well preserved.

Conclusions/Significance: This is the first finding of genome degradation in a plant symbiont and phenotypically complex cyanobacterium and one of only a few extracellular endosymbionts described showing signs of reductive genome evolution. Our findings suggest an ongoing selective streamlining of this cyanobacterial genome which has resulted in an organism devoted to nitrogen fixation and devoid of autonomous growth. The cyanobacterial symbiont of Azolla can thus be considered at the initial phase of a transition from free-living organism to a nitrogen-fixing plant entity, a transition process which may mimic what drove the evolution of chloroplasts from a cyanobacterial ancestor.

Keyword
Nostoc azollae, reductive evolution, Azolla
National Category
Microbiology
Research subject
Plant Physiology
Identifiers
urn:nbn:se:su:diva-117085 (URN)10.1371/journal.pone.0011486 (DOI)000279637100013 ()
Available from: 2015-05-06 Created: 2015-05-06 Last updated: 2017-12-04Bibliographically approved
2. Local hopping mobile DNA implicated in pseudogene formation and reductive evolution in an obligate cyanobacteria-plant symbiosis
Open this publication in new window or tab >>Local hopping mobile DNA implicated in pseudogene formation and reductive evolution in an obligate cyanobacteria-plant symbiosis
2015 (English)In: BMC Genomics, ISSN 1471-2164, E-ISSN 1471-2164, Vol. 16, 193Article in journal (Refereed) Published
Abstract [en]

Background: Insertion sequences (ISs) are approximately 1 kbp long jumping genes found in prokaryotes. ISs encode the protein Transposase, which facilitates the excision and reinsertion of ISs in genomes, making these sequences a type of class I (cut-and-paste) Mobile Genetic Elements. ISs are proposed to be involved in the reductive evolution of symbiotic prokaryotes. Our previous sequencing of the genome of the cyanobacterium 'Nostoc azollae' 0708, living in a tight perpetual symbiotic association with a plant (the water fern Azolla), revealed the presence of an eroding genome, with a high number of insertion sequences (ISs) together with an unprecedented large proportion of pseudogenes. To investigate the role of ISs in the reductive evolution of 'Nostoc azollae' 0708, and potentially in the formation of pseudogenes, a bioinformatic investigation of the IS identities and positions in 47 cyanobacterial genomes was conducted. To widen the scope, the IS contents were analysed qualitatively and quantitatively in 20 other genomes representing both free-living and symbiotic bacteria. Results: Insertion Sequences were not randomly distributed in the bacterial genomes and were found to transpose short distances from their original location (local hopping) and pseudogenes were enriched in the vicinity of IS elements. In general, symbiotic organisms showed higher densities of IS elements and pseudogenes than non-symbiotic bacteria. A total of 1108 distinct repeated sequences over 500 bp were identified in the 67 genomes investigated. In the genome of 'Nostoc azollae' 0708, IS elements were apparent at 970 locations (14.3%), with 428 being full-length. Morphologically complex cyanobacteria with large genomes showed higher frequencies of IS elements, irrespective of life style. Conclusions: The apparent co-location of IS elements and pseudogenes found in prokaryotic genomes implies earlier IS transpositions into genes. As transpositions tend to be local rather than genome wide this likely explains the proximity between IS elements and pseudogenes. These findings suggest that ISs facilitate the reductive evolution in for instance in the symbiotic cyanobacterium 'Nostoc azollae' 0708 and in other obligate prokaryotic symbionts.

Keyword
Cyanobacteria, Genomic streamlining, Insertion sequences, Local hopping, Nitrogen fixation, Pseudogenes, Symbiosis
National Category
Biological Sciences
Research subject
Plant Physiology
Identifiers
urn:nbn:se:su:diva-116609 (URN)10.1186/s12864-015-1386-7 (DOI)000351263800001 ()
Note

AuthorCount:4;

Available from: 2015-05-04 Created: 2015-04-22 Last updated: 2017-12-04Bibliographically approved
3. High transcriptional activity of insertion sequences in Baltic Sea microorganisms
Open this publication in new window or tab >>High transcriptional activity of insertion sequences in Baltic Sea microorganisms
(English)Manuscript (preprint) (Other academic)
Abstract [en]

Insertion sequences (ISs) are mobile genetic elements found in almost all prokaryotic genomes. They consist of a gene encoding a transposase, surrounded by inverted repeats. The transposase has the ability to excise the IS and insert it elsewhere in the genome, a process referred to as transposition. ISs have high copy numbers in prokaryotes inhabiting “extreme” environments, and it is proposed that their activity facilitates adaptation to environmental changes and subsequent adaptive evolution. The initial step in the transposition of an IS is the transcription of the open reading frame encoding the transposase. In an effort to evaluate the presence, activity and role of ISs in microbes of a temperate water body offering steep changes in salinity and nutrient conditions, the metatranscriptomes and metagenomes of ten water samples from the brackish water Baltic Sea were examined. ISs in the limnic Lake Torne Träsk, the marine waters off the Swedish west coast and off the coast of California were included to get perspective. The results reveal that insertion sequences make up a considerably higher fraction of the metatranscriptomes of brackish waters (0.3-1.8%) than of marine waters (0.0005-0.2%), and that the IS fraction of the metatranscriptome is commonly double that of the IS fraction of the metagenome. From these data it is concluded that ISs occupy a significant part of Baltic Sea bacterial transcription activity, in line with their proposed function as facilitators of adaptive change to changing and stressful environments.

National Category
Microbiology
Research subject
Plant Physiology
Identifiers
urn:nbn:se:su:diva-117088 (URN)
Available from: 2015-05-06 Created: 2015-05-06 Last updated: 2016-01-29Bibliographically approved

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