Dinoflagellates are a large, ecologically important phylum of marine unicellular algae. Their huge genomes make it highly challenging to decipher the genetic basis of key processes such as harmful algal bloom (HAB) formation and response to warming oceans. To address these issues, we generated a high quality genome assembly from Prorocentrum cordatum, a globally abundant, HAB forming dinoflagellate. Our analyses demonstrate massive expansion of the gene inventory to 85,849 predicted genes, primarily driven by unusually long and frequent introns and dispersed duplicates enriched for bloom relevant functions. We find that cell yield is reduced at higher culture temperatures. To understand this response, we integrated transcriptome, proteome and metabolome data and identified both a global and a temperature specific heat-stress response. The underlying metabolic changes reflect damage to photosynthesis and central metabolism. The transcriptome data show that 25% of genes are differentially expressed under heat stress, with concomittant extensive RNA editing and alternative exon usage. Multi-codon genes and transcripts for HSP70 and RuBisCo suggest a polycistronic gene organisation. Our work represents the first genome based analysis of a red tide dinoflagellate and demonstrates that temperature resilience in P. cordatum is mediated by a unique genome structure and multi-level transcriptional regulation.
Basin-scale biogeographic observations of marine pelagic pro- and eukaryotic communities are necessary to understand forces driving community composition and for providing a baseline to monitor global change. Deep sequencing of rRNA genes provides community composition at high resolution; yet, it is unclear how the choice of primers affects biogeographic patterns. Here, we re-amplified 16S rRNA genes from DNA sampled during R/V Polarstern Cruise ANT28-5 over a latitudinal transect across the Atlantic Ocean from 52°S to 47°N using universal V4-V5 primers and compared the results with those obtained previously with V5-V6 bacteria-specific primers. For validation of our results, we inferred community composition based on 16S rRNA genes of metagenomes from the same stations and single amplified genomes (SAGs) from the Global Ocean Reference Genome (GORG) database. We found that the universal V4-V5 primers retrieved SAR11 clades with similar relative proportions as those found in the GORG database while the V5-V6 primers recovered strongly diverging clade abundances. We confirmed an inverse bell-shaped distance-decay relationship and a latitudinal diversity gradient that did not decline linearly with absolute latitude in the Atlantic Ocean. Patterns were modified by sampling depth, sequencing depth, choice of primers, and abundance filtering. Especially richness patterns were not robust to methodological change. This study offers a detailed picture of the Atlantic Ocean microbiome using a universal set of PCR primers that allow for the conjunction of biogeographical patterns among organisms from different domains of life.
Marine photosynthetic microalgae are ubiquitously associated with bacteria in nature. However, the influence of these bacteria on algal cultures in bioreactors is still largely unknown. In this study, eighteen different bacterial strains were isolated from cultures of Nannochloropsis sp. CCAP211/78 in two outdoor pilot-scale tubular photobioreactors. The majority of isolates was affiliated with the classes Alphaproteobacteria and Flavobacteriia. To assess the impact of the eighteen strains on the growth of Nannochloropsis sp. CCAP211/78, 24-well plates coupled with custom-made LED boxes were used to simultaneously compare replicate axenic microalgal cultures with addition of individual bacterial isolates. Co-culturing of Nannochloropsis sp. CCAP211/78 with these strains demonstrated distinct responses, which shows that the technique we developed is an efficient method for screening the influence of harmful/beneficial bacteria. Two of the tested strains, namely a strain of Maritalea porphyrae (DMSP31) and a Labrenzia aggregata strain (YP26), significantly enhanced microalgal growth with a 14% and 12% increase of the chlorophyll concentration, respectively, whereas flavobacterial strain YP206 greatly inhibited the growth of the microalga with 28% reduction of the chlorophyll concentration. Our study suggests that algal production systems represent a 'natural' source to isolate and study microorganisms that can either benefit or harm algal cultures.
In the ocean, phytoplankton are dependent on communities of bacteria living in the phycosphere, a hot spot of metabolic and genetic exchange. Many types of interactions between phytoplankton and phycosphere bacteria have been shown, but it is unclear if the microbial communities associated with microalgae strains in culture collections are beneficial or harmful to the host strain. Here, we studied the microbial communities associated with four strains of the dinoflagellate Prorocentrum cordatum that had been isolated from distant geographical locations and maintained in culture collection for hundreds of generations. Community composition was determined by 16S rRNA gene amplicon sequencing. The dinoflagellate host strain was the strongest parameter separating communities, while growth phase, lifestyle (particle-attached versus free-living) and temperature had only a modulating effect. Although the strains had been isolated from distant locations in the Atlantic and Pacific Ocean, 14 ASVs were shared among all strains, the most abundant ones being Gilvibacter, Marivita, uncultivated Rhodobacteraceae, Marinobacter, Hyphomonadaceae, Cupriavidus, Variovorax, and Paucibacter. Adaptation to higher temperatures resulted in specific changes in each phycosphere microbiome, including increased abundance of rare community members. We then compared the growth of the four xenic cultures to that of the axenic P. cordatum CCMP1329. At 20°C, growth of the xenic cultures was similar or slower than that of CCMP1329. At 26°C, all four xenic cultures experienced a death phase, while the axenic culture stably remained in the stationary phase. At 30°C, only two of the xenic cultures were able to grow. A shift of dinoflagellate metabolism from autotrophy to mixotrophy and competition between dinoflagellate and bacteria for limiting nutrients, including essential vitamins, may contribute to these differences in growth patterns.
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