Genome Erosion in a Nitrogen-Fixing Vertically Transmitted Endosymbiotic Multicellular Cyanobacterium

Ran, Liang; Larsson, Jenny; Vigil-Stenman, Theoden; Nylander, Johan A. A.; Ininbergs, Karolina; Zheng, Weiran; Lapidus, Alla; Lowry, Stephen R.; Haselkorn, Robert; Bergman, Birgitta

doi:10.1371/journal.pone.0011486

Cited by 170 publications

(183 citation statements)

References 49 publications

(71 reference statements)

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“…When packaged into the propagules of symbiotically dispersing lichens, the Nostoc symbionts invariably experience a genetic bottleneck and their population is reduced to only a few trichomes (24)(25)(26). At the same time, the close association with a symbiotic host may promote the evolution of different traits from in freeliving cyanobacteria (27). The recurrent bottlenecks and other lichen symbiont populations shaping effects (4, 5, 28) may explain the surprising genetic and chemical diversity we now observe.…”

Section: Discussionmentioning

confidence: 79%

Cyanobacteria produce a high variety of hepatotoxic peptides in lichen symbiosis

Kaasalainen¹,

Fewer

Jokela

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

144

124

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Lichens are symbiotic associations between fungi and photosynthetic algae or cyanobacteria. Microcystins are potent toxins that are responsible for the poisoning of both humans and animals. These toxins are mainly associated with aquatic cyanobacterial blooms, but here we show that the cyanobacterial symbionts of terrestrial lichens from all over the world commonly produce microcystins. We screened 803 lichen specimens from five different continents for cyanobacterial toxins by amplifying a part of the gene cluster encoding the enzyme complex responsible for microcystin production and detecting toxins directly from lichen thalli. We found either the biosynthetic genes for making microcystins or the toxin itself in 12% of all analyzed lichen specimens. A plethora of different microcystins was found with over 50 chemical variants, and many of the variants detected have only rarely been reported from free-living cyanobacteria. In addition, high amounts of nodularin, up to 60 μg g −1 , were detected from some lichen thalli. This microcystin analog and potent hepatotoxin has previously been known only from the aquatic bloom-forming genus Nodularia. Our results demonstrate that the production of cyanobacterial hepatotoxins in lichen symbiosis is a global phenomenon and occurs in many different lichen lineages. The very high genetic diversity of the mcyE gene and the chemical diversity of microcystins suggest that lichen symbioses may have been an important environment for diversification of these cyanobacteria.Nostoc | Peltigera | cyanolichen | secondary metabolites | chemical defence

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Section: Discussionmentioning

confidence: 79%

Cyanobacteria produce a high variety of hepatotoxic peptides in lichen symbiosis

Kaasalainen¹,

Fewer

Jokela

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

144

124

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“…Thus, the evolutionary history of DNA replication from a cyanobacterial to a plastid system can be discerned from genetic evidence. Interestingly, dnaA is the only gene that is not conserved between red algae, the cyanobacterial symbiont Diversification of cyanobacterial DNA replication R Ohbayashi et al Nostoc azollae (Ran et al, 2010) and the spheroid bodies (Nakayama et al, 2014) of diatoms. We have shown that cyanobacteria have the capacity to shift the DNA replication initiation system from chromosomal to plasmid type by dnaA deletion.…”

Section: Discussionmentioning

confidence: 99%

“…As such, DnaA is essential for DNA replication initiation in most bacteria. Indeed, with the exception of certain symbiotic species, there are no known free-living, DnaA-independent bacteria (Akman et al, 2002;Ran et al, 2010;Nakayama et al, 2014).…”

Section: Introductionmentioning

confidence: 99%

“…In contrast, the dnaA gene is not essential for cell viability in Synechocystis (Richter et al, 1998), although additional characteristics were not addressed. The dnaA gene is inactivated by a transposon insertion in the symbiotic cyanobacterium Nostoc azolla (Akman et al, 2002) and is not conserved in the diatom endosymbiont that is of cyanobacterial origin (termed a spheroid body) with a 2.7-Mb genome (Ran et al, 2010). Moreover, recent study suggested that most of the DNA replication enzymes in chloroplast originated from cyanobacteria and others , and the vestige of symbiotic evolution was observed.…”

Section: Introductionmentioning

confidence: 99%

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Diversification of DnaA dependency for DNA replication in cyanobacterial evolution

et al. 2015

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Regulating DNA replication is essential for all living cells. The DNA replication initiation factor DnaA is highly conserved in prokaryotes and is required for accurate initiation of chromosomal replication at oriC. DnaA-independent free-living bacteria have not been identified. The dnaA gene is absent in plastids and some symbiotic bacteria, although it is not known when or how DnaA-independent mechanisms were acquired. Here, we show that the degree of dependency of DNA replication on DnaA varies among cyanobacterial species. Deletion of the dnaA gene in Synechococcus elongatus PCC 7942 shifted DNA replication from oriC to a different site as a result of the integration of an episomal plasmid. Moreover, viability during the stationary phase was higher in dnaA disruptants than in wild-type cells. Deletion of dnaA did not affect DNA replication or cell growth in Synechocystis sp. PCC 6803 or Anabaena sp. PCC 7120, indicating that functional dependency on DnaA was already lost in some nonsymbiotic cyanobacterial lineages during diversification. Therefore, we proposed that cyanobacteria acquired DnaA-independent replication mechanisms before symbiosis and such an ancestral cyanobacterium was the sole primary endosymbiont to form a plastid precursor.

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“…Symbiosis is not restricted to unicellular endosymbionts. The vertically transmitted endosymbiont (Anabaena) of the pteridophyte Azolla, which was reduced to an organism devoted to nitrogen fixation, is a multicellular cyanobacterium [89]. Another example is the angiosperm Gunnera manicata that uses the nitrogen provided by the filamentous symbiont (Nostoc punctiforme) and continues growing under N-limited conditions in the presence of the symbiont [90].…”

Section: Why: the Physiological Context Of Plastid Originmentioning

confidence: 99%

Plastid origin: who, when and why?

Roettger

Zimorski

et al. 2014

Acta Soc Bot Pol

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Plastid origin: 110 years since MereschkowskyPlastids are eukaryotic metabolic compartments responsible for photosynthesis [1] and a variety of metabolic functions including the biosynthesis of amino acids [2], nucleotides [3], lipids [4], and cofactors [5]. The importance of plastids to photosynthetic lineages of eukaryotes cannot be overstated. In 1905, Mereschkowsky proposed a fully articulated version of endosymbiotic theory positing that plastids originated from cyanobacteria that came to reside as symbionts in eukaryotic cells [6,7]. The theory did not make its way into mainstream biological thinking until it was revived in a synthesis by Margulis [8,9] that also incorporated Wallin's [10] -and Paul Portier's (published in French, cited in Sapp [11]) -ideas about endosymbiotic theory for mitochondrial origin, yet adorned by Margulis' own suggestion of a spirochaete origin of flagella. The spirochaete story never took hold, leaving endosymbiotic theory with three main players: the plastid, the mitochondrion, and its host, which is now understood to be an archaeon [12]. Well into the 1970s, resistance to the concept of endosymbiosis for the origin of plastids (and mitochondria) was stiff [13][14][15].With the availability of protein and DNA sequences, of which Mereschkowsky knew nothing, strong evidence had accumulated by the early 1980s that plastids originated through endosymbiosis from cyanobacteria, rather than autogenously [16]. However, there have been recurrent suggestions, starting with Mereschkowsky [6] and tracing into the 1970's [17], that there were several independent origins of plastids from cyanobacteria. Today it is widely, but not universally [18,19], accepted that plastids had a single origin. The strongest evidence for that view is that the protein import machinery, a good marker for endosymbiotic events [20], in the three lineages of Archaeplastida -eukaryotes with primary plastids [21] -consists of homologous host-originated components [22][23][24], which would not be the case had plastids in those lineages arisen from independent cyanobacterial symbioses.Genomics has enriched our understanding of plastid origin. We now know that the plastid genome has undergone extreme reduction while leaving its imprints in the nuclear genome through endosymbiotic gene transfer [25,26] and that plastids have spread across eukaryotes through symbiosis and become secondary and tertiary plastids [27]. Genomic data also supports the case for a single plastid origin. Despite some concerns about incomplete sampling and phylogenetic artifacts [18], recent analyses from different groups, incorporating improved phylogenetic algorithms and sampling of cyanobacteria, provide two lines of evidence, in addition to * Corresponding author. Email: bill@hhu.deHandling Editor: Andrzej Bodył INVITED REVIEW Acta Soc Bot Pol 83(4): 281-289 DOI: 10.5586/asbp.2014.045 Received: 2014-11-20 Accepted: 2014-12-04 Published electronically: 2014 Plastid origin: who, when and why?Chuan Ku, Mayo Roettger, Verena Zimorski, Shijulal...

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Genome Erosion in a Nitrogen-Fixing Vertically Transmitted Endosymbiotic Multicellular Cyanobacterium

Cited by 170 publications

References 49 publications

Cyanobacteria produce a high variety of hepatotoxic peptides in lichen symbiosis

Cyanobacteria produce a high variety of hepatotoxic peptides in lichen symbiosis

Diversification of DnaA dependency for DNA replication in cyanobacterial evolution

Plastid origin: who, when and why?

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