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TitleGenome analysis of the freshwater planktonic Vulcanococcus limneticus sp. nov. reveals horizontal transfer of nitrogenase operon and alternative pathways of nitrogen utilization
AbstractBackground: Many cyanobacteria are capable of fixing atmospheric nitrogen, playing a crucial role in biogeochemical cycling. Little is known about freshwater unicellular cyanobacteria Synechococcus spp. at the genomic level, despite being recognised of considerable ecological importance in aquatic ecosystems. So far, it has not been shown whether these unicellular picocyanobacteria have the potential for nitrogen fixation. Here, we present the draft-genome of the new pink-pigmented Synechococcus-like strain Vulcanococcus limneticus. sp. nov., isolated from the volcanic Lake Albano (Central Italy). Results: The novel species Vulcanococcus limneticus sp. nov. falls inside the sub-cluster 5.2, close to the estuarine/marine strains in a maximum-likelihood phylogenetic tree generated with 259 marker genes with representatives from marine, brackish, euryhaline and freshwater habitats. V.limneticus sp. nov. possesses a complete nitrogenase and nif operon. In an experimental setup under nitrogen limiting and non-limiting conditions, growth was observed in both cases. However, the nitrogenase genes (nifHDK) were not transcribed, i.e., V.limneticus sp. nov. did not fix nitrogen, but instead degraded the phycobilisomes to produce sufficient amounts of ammonia. Moreover, the strain encoded many other pathways to incorporate ammonia, nitrate and sulphate, which are energetically less expensive for the cell than fixing nitrogen. The association of the nif operon to a genomic island, the relatively high amount of mobile genetic elements (52 transposases) and the lower observed GC content of V.limneticus sp. nov. nif operon (60.54%) compared to the average of the strain (68.35%) support the theory that this planktonic strain may have obtained, at some point of its evolution, the nif operon by horizontal gene transfer (HGT) from a filamentous or heterocystous cyanobacterium. Conclusions: In this study, we describe the novel species Vulcanococcus limneticus sp. nov., which possesses a complete nif operon for nitrogen fixation. The finding that in our experimental conditions V.limneticus sp. nov. did not express the nifHDK genes led us to reconsider the actual ecological meaning of these accessory genes located in genomic island that have possibly been acquired via HGT.
SourceBMC genomics 19 (1)
KeywordsGenomic islandHorizontal gene transfer (HGT)Nitrogen fixationNitrogenase genesPicocyanobacteriaVulcanococcus limneticus sp. nov.
JournalBMC genomics
EditorBioMed Central,, London, Regno Unito
Year2018
TypeArticolo in rivista
DOI10.1186/s12864-018-4648-3
AuthorsDi Cesare A.; Cabello-Yeves P.J.; Chrismas N.A.M.; Sanchez-Baracaldo P.; Salcher M.M.; Callieri C.
Text392824 2018 10.1186/s12864 018 4648 3 Scopus 2 s2.0 85045458617 ISI Web of Science WOS 000430805000007 Genomic island Horizontal gene transfer HGT Nitrogen fixation Nitrogenase genes Picocyanobacteria Vulcanococcus limneticus sp. nov. Genome analysis of the freshwater planktonic Vulcanococcus limneticus sp. nov. reveals horizontal transfer of nitrogenase operon and alternative pathways of nitrogen utilization Di Cesare A.; Cabello Yeves P.J.; Chrismas N.A.M.; Sanchez Baracaldo P.; Salcher M.M.; Callieri C. National Research Council CNR ISE, Largo Tonolli 50, Verbania, 28922, , Italy; University of Genoa, Department of Earth, Environmental, and Life Sciences, Genoa, 16132, , Italy; Universidad Miguel Hernandez, Evolutionary Genomics Group, Departamento de Produccion Vegetal y Microbiologia, San Juan de Alicante, , Spain; School of Geographical Sciences, University of Bristol, Bristol, BS8 1SS, , United Kingdom; Marine Biological Association of the United Kingdom, The Laboratory, Citadel Hill, Plymouth, , United Kingdom; Limnological Station, Institute of Plant and Microbial Biology, University of Zurich, Kilchberg, , Switzerland Background Many cyanobacteria are capable of fixing atmospheric nitrogen, playing a crucial role in biogeochemical cycling. Little is known about freshwater unicellular cyanobacteria Synechococcus spp. at the genomic level, despite being recognised of considerable ecological importance in aquatic ecosystems. So far, it has not been shown whether these unicellular picocyanobacteria have the potential for nitrogen fixation. Here, we present the draft genome of the new pink pigmented Synechococcus like strain Vulcanococcus limneticus. sp. nov., isolated from the volcanic Lake Albano Central Italy . Results The novel species Vulcanococcus limneticus sp. nov. falls inside the sub cluster 5.2, close to the estuarine/marine strains in a maximum likelihood phylogenetic tree generated with 259 marker genes with representatives from marine, brackish, euryhaline and freshwater habitats. V.limneticus sp. nov. possesses a complete nitrogenase and nif operon. In an experimental setup under nitrogen limiting and non limiting conditions, growth was observed in both cases. However, the nitrogenase genes nifHDK were not transcribed, i.e., V.limneticus sp. nov. did not fix nitrogen, but instead degraded the phycobilisomes to produce sufficient amounts of ammonia. Moreover, the strain encoded many other pathways to incorporate ammonia, nitrate and sulphate, which are energetically less expensive for the cell than fixing nitrogen. The association of the nif operon to a genomic island, the relatively high amount of mobile genetic elements 52 transposases and the lower observed GC content of V.limneticus sp. nov. nif operon 60.54% compared to the average of the strain 68.35% support the theory that this planktonic strain may have obtained, at some point of its evolution, the nif operon by horizontal gene transfer HGT from a filamentous or heterocystous cyanobacterium. Conclusions In this study, we describe the novel species Vulcanococcus limneticus sp. nov., which possesses a complete nif operon for nitrogen fixation. The finding that in our experimental conditions V.limneticus sp. nov. did not express the nifHDK genes led us to reconsider the actual ecological meaning of these accessory genes located in genomic island that have possibly been acquired via HGT. 19 Published version http //www.scopus.com/inward/record.url eid=2 s2.0 85045458617 partnerID=q2rCbXpz Articolo 2018_BMC_Genomics_19_259.pdf Articolo in rivista BioMed Central, 1471 2164 BMC genomics BMC genomics BMC genomics BMC genomics Genomics cristiana.callieri CALLIERI CRISTIANA