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Single-cell genomics unveiled a cryptic cyanobacterial lineage with a worldwide distribution hidden by a dinoflagellate host.

ABSTRACT: Cyanobacteria are one of the most important contributors to oceanic primary production and survive in a wide range of marine habitats. Much effort has been made to understand their ecological features, diversity, and evolution, based mainly on data from free-living cyanobacterial species. In addition, symbiosis has emerged as an important lifestyle of oceanic microbes and increasing knowledge of cyanobacteria in symbiotic relationships with unicellular eukaryotes suggests their significance in understanding the global oceanic ecosystem. However, detailed characteristics of these cyanobacteria remain poorly described. To gain better insight into marine cyanobacteria in symbiosis, we sequenced the genome of cyanobacteria collected from a cell of a pelagic dinoflagellate that is known to host cyanobacterial symbionts within a specialized chamber. Phylogenetic analyses using the genome sequence revealed that the cyanobacterium represents an underdescribed lineage within an extensively studied, ecologically important group of marine cyanobacteria. Metagenomic analyses demonstrated that this cyanobacterial lineage is globally distributed and strictly coexists with its host dinoflagellates, suggesting that the intimate symbiotic association allowed the cyanobacteria to escape from previous metagenomic studies. Furthermore, a comparative analysis of the protein repertoire with related species indicated that the lineage has independently undergone reductive genome evolution to a similar extent as Prochlorococcus, which has the most reduced genomes among free-living cyanobacteria. Discovery of this cyanobacterial lineage, hidden by its symbiotic lifestyle, provides crucial insights into the diversity, ecology, and evolution of marine cyanobacteria and suggests the existence of other undiscovered cryptic cyanobacterial lineages.

SUBMITTER: Nakayama T

PROVIDER: S-EPMC6689939 | biostudies-literature | 2019 Aug

REPOSITORIES: biostudies-literature

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Single-cell genomics unveiled a cryptic cyanobacterial lineage with a worldwide distribution hidden by a dinoflagellate host.

Nakayama Takuro T Nomura Mami M Takano Yoshihito Y Tanifuji Goro G Shiba Kogiku K Inaba Kazuo K Inagaki Yuji Y Kawata Masakado M

Proceedings of the National Academy of Sciences of the United States of America 20190624 32

Cyanobacteria are one of the most important contributors to oceanic primary production and survive in a wide range of marine habitats. Much effort has been made to understand their ecological features, diversity, and evolution, based mainly on data from free-living cyanobacterial species. In addition, symbiosis has emerged as an important lifestyle of oceanic microbes and increasing knowledge of cyanobacteria in symbiotic relationships with unicellular eukaryotes suggests their significance in u ...[more]

PMID: 31235587

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Project description:BackgroundThe Rhynchosporium species complex consists of hemibiotrophic fungal pathogens specialized to different sweet grass species including the cereal crops barley and rye. A sexual stage has not been described, but several lines of evidence suggest the occurrence of sexual reproduction. Therefore, a comparative genomics approach was carried out to disclose the evolutionary relationship of the species and to identify genes demonstrating the potential for a sexual cycle. Furthermore, due to the evolutionary very young age of the five species currently known, this genus appears to be well-suited to address the question at the molecular level of how pathogenic fungi adapt to their hosts.ResultsThe genomes of the different Rhynchosporium species were sequenced, assembled and annotated using ab initio gene predictors trained on several fungal genomes as well as on Rhynchosporium expressed sequence tags. Structures of the rDNA regions and genome-wide single nucleotide polymorphisms provided a hypothesis for intra-genus evolution. Homology screening detected core meiotic genes along with most genes crucial for sexual recombination in ascomycete fungi. In addition, a large number of cell wall-degrading enzymes that is characteristic for hemibiotrophic and necrotrophic fungi infecting monocotyledonous hosts were found. Furthermore, the Rhynchosporium genomes carry a repertoire of genes coding for polyketide synthases and non-ribosomal peptide synthetases. Several of these genes are missing from the genome of the closest sequenced relative, the poplar pathogen Marssonina brunnea, and are possibly involved in adaptation to the grass hosts. Most importantly, six species-specific genes coding for protein effectors were identified in R. commune. Their deletion yielded mutants that grew more vigorously in planta than the wild type.ConclusionBoth cryptic sexuality and secondary metabolites may have contributed to host adaptation. Most importantly, however, the growth-retarding activity of the species-specific effectors suggests that host adaptation of R. commune aims at extending the biotrophic stage at the expense of the necrotrophic stage of pathogenesis. Like other apoplastic fungi Rhynchosporium colonizes the intercellular matrix of host leaves relatively slowly without causing symptoms, reminiscent of the development of endophytic fungi. Rhynchosporium may therefore become an object for studying the mutualism-parasitism transition.

Project description:BackgroundDinoflagellates have the potential to pose severe ecological and economic damages to aquatic ecosystems. It is therefore largely needed to understand the causes and consequences of distribution patterns of dinoflagellate communities in order to manage potential environmental problems. However, a majority of studies have focused on marine ecosystems, while the geographical distribution patterns of dinoflagellate communities and associated determinants in freshwater ecosystems remain unexplored, particularly in running water ecosystems such as rivers and streams.MethodsHere we utilized multiple linear regression analysis and combined information on species composition recovered by high-throughput sequencing and spatial and environmental variables to analyze the distribution patterns of dinoflagellate communities along the Songhua River.ResultsAfter high-throughput sequencing, a total of 490 operational taxonomic units (OTUs) were assigned to dinoflagellates, covering seven orders, 13 families and 22 genera. Although the sample sites were grouped into three distinctive clusters with significant difference (p < 0.05) in environmental variables, OTUs-based dinoflagellate communities among the three clusters showed no significant difference (p > 0.05). Among all 24 environmental factors, two environmental variables, including NO3-N and total dissolved solids (TDS), were selected as the significantly influential factors (p < 0.05) on the distribution patterns of dinoflagellate communities based on forward selection. The redundancy analysis (RDA) model showed that only a small proportion of community variation (6.1%) could be explained by both environmental (NO3-N and TDS) and dispersal predictors (watercourse distance) along the River. Variance partitioning revealed a larger contribution of local environmental factors (5.85%) than dispersal (0.50%) to the total variation of dinoflagellate communities.DiscussionOur findings indicated that in addition to the two quantifiable processes in this study (species sorting and dispersal), more unquantifiable stochastic processes such as temporal extinction and colonization events due to rainfall may be responsible for the observed geographical distribution of the dinoflagellate community along the Songhua River. Results obtained in this study suggested that deeper investigations covering different seasons are needed to understand the causes and consequences of geographical distribution patterns of dinoflagellate biodiversity in river ecosystems.

Dataset Information

Single-cell genomics unveiled a cryptic cyanobacterial lineage with a worldwide distribution hidden by a dinoflagellate host.

Publications

Single-cell genomics unveiled a cryptic cyanobacterial lineage with a worldwide distribution hidden by a dinoflagellate host.

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