Evolving interactions between diazotrophic cyanobacterium and phage mediate nitrogen release and host competitive ability

Cairns, Johannes; Coloma, Sebastián; Sivonen, Kaarina; Hiltunen, Teppo

doi:10.1098/rsos.160839

Cited by 17 publications

(25 citation statements)

References 67 publications

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“…We have here shown that cyanophages have a different beta diversity in hypoxic-anoxic sediment compared to oxic, and are actively infecting cyanobacteria triggering the CRISPR/Cas system. We observed cyanobacterial N 2 xation in the hypoxic-anoxic sediment, and it is therefore likely that viral lysis of these cells contribute carbon, phosphorus, and nitrogen to other microorganisms [33,34]. The bacterial uptake of lysed material has been shown to be especially important in oligotrophic environments were nutrients are scarce [52], and this further suggests that viruses might have an important role in the studied dead zone sediments as they have been shown to be low or depleted in nitrate [43].…”

Section: Discussionmentioning

confidence: 59%

“…Cyanophages are viruses that are known to infect cyanobacteria and after infection lytic cyanophages eventually lyse the host cell [30][31][32], and thus contribute to the release of carbon and nutrients into the environment [33,34]. Furthermore, cyanophages might increase the decay of pelagic cyanobacteria and increase the amount sinking down towards the seabed through increased particle formation caused by viral lysis [35].…”

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

Cyanobacterial taxonomy, metabolism, and cyanophage association in dark and anoxic sediment

Broman

Holmfeldt

Bonaglia

et al. 2019

Preprint

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Background Cyanobacteria are photosynthetic ancient bacteria ubiquitous in terrestrial and aquatic environments. Even though they carry a photosynthesis apparatus they are known to survive in dark environments. Cyanophages are viruses that infect and lyse cyanobacterial cells, adding bioavailable carbon and nutrients into the environment. Here we present the first study that investigate the metabolic spectrum of cyanobacteria in dark and anoxic environments, as well as their associated cyanophages. We sampled surface sediments during April 2018 located along a water depth gradient of 60–210 m—representing oxic, hypoxic and anoxic conditions—in the largest dead zone in the world. We combined metagenomic and total RNA sequencing to investigate cyanobacterial taxonomy, activity and their associated cyanophages. Results Cyanobacteria were detected at all four stations (n = 3 per station) along the sampled gradient, including the anoxic sediment. Top active genera in the anoxic sediment included Anabaena (19% RNA data), Synechococcus (16%), and Cyanobium (5%). The mRNA data showed that cyanobacteria were surviving through i) anaerobic carbon metabolism indicated by glycolysis plus fatty acid biosynthesis, and ii) nitrogen (N2) fixation (likely by heterocystous Anabaena). Interestingly, cyanobacteria were also actively transcribing photosynthesis, phytochromes, and gas vesicle genes. Cyanophages were also detected at all stations, and compared to the oxic sediment had a different beta diversity in the hypoxic-anoxic sediment. Moreover, our results show that these cyanophages infect cyanobacteria affecting the photosystem and phosphate regulation of cyanobacteria. Conclusions Cyanobacteria were found to transcribe genes for photosynthesis, phytochromes, and gas vesicles and this suggests that cyanobacteria are trying to ascend to the surface waters. The difference in cyanophage beta diversity between oxic and hypoxic-anoxic sediment suggests that anaerobic cyanobacteria select for specific cyanophages. Cyanobacteria are known to fuel oxygen depleted benthic ecosystems with phosphorous (so called internal loading), and our study suggests that cyanophage-controlled lysis of cyanobacteria likely provides a source of nitrogen. Photosynthetic cyanobacteria are commonly thought to have been essential in the great oxygenation event on Earth ca. 2.4 billion years ago. Our results suggest that active cyanobacteria might also provide nutrients (via N2 fixation and viral lysis) in dark and anoxic environments.

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Section: Discussionmentioning

confidence: 59%

Section: Introductionmentioning

confidence: 99%

Cyanobacterial taxonomy, metabolism, and cyanophage association in dark and anoxic sediment

Broman

Holmfeldt

Bonaglia

et al. 2019

Preprint

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“…Both strains had been successfully cultured under similar conditions previously (Cairns et al. , Coloma et al. ).…”

Section: Methodsmentioning

confidence: 98%

“…Recently, we demonstrated that phage resistance evolution can alter phage‐mediated nitrogen release in filamentous cyanobacterial populations but potential larger, community‐level effects remain unclear (Cairns et al. , Coloma et al. ).…”

Section: Introductionmentioning

confidence: 99%

Frequency of virus‐resistant hosts determines experimental community dynamics

Coloma

Gaedke

Sivonen

et al. 2018

Ecology

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Parasites, such as bacterial viruses (phages), can have large effects on host populations both at the ecological and evolutionary levels. In the case of cyanobacteria, phages can reduce primary production and infected hosts release intracellular nutrients influencing planktonic food web structure, community dynamics, and biogeochemical cycles. Cyanophages may be of great importance in aquatic food webs during large cyanobacterial blooms unless the host population becomes resistant to phage infection. The consequences on plankton community dynamics of the evolution of phage resistance in bloom forming cyanobacterial populations are still poorly studied. Here, we examined the effect of different frequencies of a phage‐resistant genotype within a filamentous nitrogen‐fixing Nodularia spumigena population on an experimental plankton community. Three Nodularia populations with different initial frequencies (0%, 5%, and 50%) of phage‐resistant genotypes were inoculated in separate treatments with the phage 2AV2, the green alga Chlorella vulgaris, and the rotifer Brachionus plicatilis, which formed the experimental plankton community subjected to either nitrogen‐limited or nitrogen‐rich conditions. We found that the frequency of the phage‐resistant Nodularia genotype determined experimental community dynamics. Cyanobacterial populations with a high frequency (50%) of the phage‐resistant genotype dominated the cultures despite the presence of phages, retaining most of the intracellular nitrogen in the plankton community. In contrast, populations with low frequencies (0% and 5%) of the phage‐resistant genotype were lysed and reduced to extinction by the phage, transferring the intracellular nitrogen held by Nodularia to Chlorella and rotifers, and allowing Chlorella to dominate the communities and rotifers to survive. This study shows that even though phages represent minuscule biomass, they can have key effects on community composition and eco‐evolutionary feedbacks in plankton communities.

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“…Cyanophages are viruses that are known to infect cyanobacteria and after infection lytic cyanophages eventually lyse the host cell [32][33][34], and thus contribute to the release of carbon and nutrients into the environment [35,36]. Furthermore, cyanophages might increase the decay of pelagic cyanobacteria and increase the amount sinking down towards the seabed through increased particle formation caused by viral lysis [37].…”

Section: Introductionmentioning

confidence: 99%

Cyanobacterial taxonomy, metabolism, and cyanophage association in dark and anoxic sediment

Broman

Holmfeldt

Bonaglia

et al. 2020

Preprint

View full text Add to dashboard Cite

BackgroundCyanobacteria are photosynthetic ancient bacteria ubiquitous in terrestrial and aquatic environments. Even though they carry a photosynthesis apparatus they are known to survive in dark environments. Cyanophages are viruses that infect and lyse cyanobacterial cells, adding bioavailable carbon and nutrients into the environment. Here we present the first study that investigate the metabolic spectrum of cyanobacteria in dark and anoxic environments, as well as their associated cyanophages. We sampled surface sediments during April 2018 located along a water depth gradient of 60–210 m—representing oxic, hypoxic and anoxic conditions—in the largest dead zone in the world (Baltic Sea). We combined metagenomic and RNA-seq to investigate cyanobacterial taxonomy, activity and their associated cyanophages.ResultsCyanobacteria were detected at all four stations (n = 3 per station) along the sampled gradient, including the anoxic sediment. Top genera in the anoxic sediment included Anabaena (19% RNA data), Synechococcus (16%), and Cyanobium (5%). The mRNA data showed that cyanobacteria were surviving through i) anaerobic carbon metabolism indicated by glycolysis plus fatty acid biosynthesis, and ii) nitrogen (N2) fixation (likely by heterocystous Anabaena). Interestingly, in the mRNA data cyanobacteria were also transcribing photosynthesis, phytochromes, and gas vesicle genes. Cyanophages were detected at all stations, and compared to the oxic sediment had a different beta diversity in the hypoxic-anoxic sediment. Moreover, our results show that these cyanophages can infect cyanobacteria affecting the photosystem and phosphate regulation.ConclusionsCyanobacteria were found to transcribe genes for photosynthesis, phytochromes, and gas vesicles and this suggests that cyanobacteria try to ascend to the surface waters. The difference in cyanophage beta diversity between oxic and hypoxic-anoxic sediment suggests that anaerobic cyanobacteria select for specific cyanophages. Cyanobacteria are known to fuel oxygen depleted benthic ecosystems with phosphorous (so called internal loading), and our study suggests that cyanophage-controlled lysis of cyanobacteria likely provides a source of nitrogen. Our results suggest that cyanobacteria might also provide nutrients via N2 fixation and viral lysis in dark and anoxic environments.

show abstract

Evolving interactions between diazotrophic cyanobacterium and phage mediate nitrogen release and host competitive ability

Cited by 17 publications

References 67 publications

Cyanobacterial taxonomy, metabolism, and cyanophage association in dark and anoxic sediment

Cyanobacterial taxonomy, metabolism, and cyanophage association in dark and anoxic sediment

Frequency of virus‐resistant hosts determines experimental community dynamics

Cyanobacterial taxonomy, metabolism, and cyanophage association in dark and anoxic sediment

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