The mesopelagic anoxic Black Sea as an unexpected habitat for <i>Synechococcus</i> challenges our understanding of global “deep red fluorescence”

Callieri, Cristiana; Slabakova, Violeta; Dzhembekova, Nina; Slabakova, Nataliya; Peneva, Elisaveta; Cabello‐Yeves, Pedro J.; Cesare, Andrea Di; Eckert, Ester M.; Bertoni, Roberto; Corno, Gianluca; Salcher, Michaela M.; Kamburska, Lyudmila; Bertoni, Filippo; Moncheva, Snejana

doi:10.1038/s41396-019-0378-z

Cited by 43 publications

(68 citation statements)

References 57 publications

(67 reference statements)

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“…The October 2014 spring bloom appears to have extended into the anoxic interface where the Chlorobium abundance was at its lowest (see below). It is possible that fermentative abilities allow Synechococcus to survive in dark and anoxic conditions, as inferred for Synechococcus in the Black Sea [ 23 ]. Ace Lake Synechococcu s encodes enzymes potentially involved in fermentation, including synthesis and mobilization of glycogen [ 23 , 24 ], the latter coupled to hydrogen production using a Hox hydrogenase [ 25 ] or lactate production using D-lactate dehydrogenase [ 23 ].…”

Section: Resultsmentioning

confidence: 99%

Influence of the polar light cycle on seasonal dynamics of an Antarctic lake microbial community

et al. 2020

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Background Cold environments dominate the Earth’s biosphere and microbial activity drives ecosystem processes thereby contributing greatly to global biogeochemical cycles. Polar environments differ to all other cold environments by experiencing 24-h sunlight in summer and no sunlight in winter. The Vestfold Hills in East Antarctica contains hundreds of lakes that have evolved from a marine origin only 3000–7000 years ago. Ace Lake is a meromictic (stratified) lake from this region that has been intensively studied since the 1970s. Here, a total of 120 metagenomes representing a seasonal cycle and four summers spanning a 10-year period were analyzed to determine the effects of the polar light cycle on microbial-driven nutrient cycles. Results The lake system is characterized by complex sulfur and hydrogen cycling, especially in the anoxic layers, with multiple mechanisms for the breakdown of biopolymers present throughout the water column. The two most abundant taxa are phototrophs (green sulfur bacteria and cyanobacteria) that are highly influenced by the seasonal availability of sunlight. The extent of the Chlorobium biomass thriving at the interface in summer was captured in underwater video footage. The Chlorobium abundance dropped from up to 83% in summer to 6% in winter and 1% in spring, before rebounding to high levels. Predicted Chlorobium viruses and cyanophage were also abundant, but their levels did not negatively correlate with their hosts. Conclusion Over-wintering expeditions in Antarctica are logistically challenging, meaning insight into winter processes has been inferred from limited data. Here, we found that in contrast to chemolithoautotrophic carbon fixation potential of Southern Ocean Thaumarchaeota, this marine-derived lake evolved a reliance on photosynthesis. While viruses associated with phototrophs also have high seasonal abundance, the negative impact of viral infection on host growth appeared to be limited. The microbial community as a whole appears to have developed a capacity to generate biomass and remineralize nutrients, sufficient to sustain itself between two rounds of sunlight-driven summer-activity. In addition, this unique metagenome dataset provides considerable opportunity for future interrogation of eukaryotes and their viruses, abundant uncharacterized taxa (i.e. dark matter), and for testing hypotheses about endemic species in polar aquatic ecosystems.

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Section: Resultsmentioning

confidence: 99%

Influence of the polar light cycle on seasonal dynamics of an Antarctic lake microbial community

et al. 2020

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“…T. elongatus BP1 78 6.8 1.09 0.0036 Onsen information sheet* Cyanobacteria are found in a wide range of environments -the knowledge of which continues to expand (Whitton, 1992;Puente-Sánchez et al, 2018;Callieri et al, 2019). As a single phylogenetic group, members of the Thermosynechococcus genus have been documented to inhabit a range of chemical environments, some of which might be similar to places and times on the early Earth.…”

Section: Tokyo Japan)mentioning

confidence: 99%

TheThermosynechococcusgenus: wide environmental distribution, but a highly conserved genomic core

Prondzinsky

Berkemer

Ward

et al. 2020

Preprint

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Cyanobacteria thrive in very diverse environments. In Earth history however, delayed oxygenation has raised questions of growth limitation in ancient environmental conditions. As a single genus, the Thermosynechococcus are known to be cosmopolitan and live in chemically diverse habitats. To understand the genetic basis for this, we compared the protein coding component of Thermosynechococcus genomes. Supplementing the known genetic diversity of Thermosynechococcus, we report draft metagenome-assembled genomes of two Thermosynechococcus recovered from ferrous carbonate hot springs in Japan. We find that as a genus, Thermosynechococcus is genomically conserved, having a small pan-genome with few accessory genes per individual strain and only 18 protein clusters appearing in all Thermosynechococcus but not in any other cyanobacteria in our analysis. Furthermore, by comparing orthologous protein groups, including an analysis of genes encoding proteins with an iron related function (uptake, storage or utilization), no clear differences in genetic content, or adaptive mechanisms could be detected between genus members, despite the range of environments they inhabit. Overall, our results highlight a seemingly innate ability for Thermosynechococcus to inhabit diverse habitats without having undergone substantial genomic adaptation to accommodate this. The finding of Thermosynechococcus in both hot and high iron environments without adaptation recognizable from the perspective of protein coding genes has implications for understanding the basis of thermophily within this clade, and also suggests that ferrous iron in ancient oceans may not have inhibited the proliferation of Cyanobacteria on Earth. The conserved core genome may be indicative of an allopatric lifestyle - or reduced genetic complexity of hot spring habitats relative to other environments.

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“…Contrary to Anabaena, the other top genera detected in the hypoxic-anoxic sediment Cyanobium and Synechococcus are not known to form akinetes [46]. However, Synechococcus has been shown to survive in anoxic and dark waters in the Black Sea with strong indications of being capable of fermentation [47]. It is therefore possible to these cyanobacteria survives in the dark and anoxic sediment anaerobically.…”

Section: Discussionmentioning

confidence: 99%

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

Broman

Holmfeldt

Bonaglia

et al. 2020

Preprint

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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.

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The mesopelagic anoxic Black Sea as an unexpected habitat for Synechococcus challenges our understanding of global “deep red fluorescence”

Cited by 43 publications

References 57 publications

Influence of the polar light cycle on seasonal dynamics of an Antarctic lake microbial community

Influence of the polar light cycle on seasonal dynamics of an Antarctic lake microbial community

TheThermosynechococcusgenus: wide environmental distribution, but a highly conserved genomic core

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

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