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  1. Acidification of the ocean due to high atmospheric CO 2 levels may increase the resilience of diatoms causing dramatic shifts in abiotic and biotic cycles with lasting implications on marine ecosystems. Here, we report a potential bioindicator of a shift in the resilience of a coastal and centric model diatom Thalassiosira pseudonana under elevated CO 2 . Specifically, we have discovered, through EGFP-tagging, a plastid membrane localized putative Na + (K + )/H + antiporter that is significantly upregulated at >800 ppm CO 2 , with a potentially important role in maintaining pH homeostasis. Notably, transcript abundance of this antiporter gene was relatively low and constant over the diel cycle under contemporary CO 2 conditions. In future acidified oceanic conditions, dramatic oscillation with >10-fold change between nighttime (high) and daytime (low) transcript abundances of the antiporter was associated with increased resilience of T. pseudonana . By analyzing metatranscriptomic data from the Tara Oceans project, we demonstrate that phylogenetically diverse diatoms express homologs of this antiporter across the globe. We propose that the differential between night- and daytime transcript levels of the antiporter could serve as a bioindicator of a shift in the resilience of diatoms in response to high CO 2 conditions in marine environments. 
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  2. Abstract

    Early evolution of mutualism is characterized by big and predictable adaptive changes, including the specialization of interacting partners, such as through deleterious mutations in genes not required for metabolic cross-feeding. We sought to investigate whether these early mutations improve cooperativity by manifesting in synergistic epistasis between genomes of the mutually interacting species. Specifically, we have characterized evolutionary trajectories of syntrophic interactions of Desulfovibrio vulgaris (Dv) with Methanococcus maripaludis (Mm) by longitudinally monitoring mutations accumulated over 1000 generations of nine independently evolved communities with analysis of the genotypic structure of one community down to the single-cell level. We discovered extensive parallelism across communities despite considerable variance in their evolutionary trajectories and the perseverance within many evolution lines of a rare lineage of Dv that retained sulfate-respiration (SR+) capability, which is not required for metabolic cross-feeding. An in-depth investigation revealed that synergistic epistasis across pairings of Dv and Mm genotypes had enhanced cooperativity within SR− and SR+ assemblages, enabling their coexistence within the same community. Thus, our findings demonstrate that cooperativity of a mutualism can improve through synergistic epistasis between genomes of the interacting species, enabling the coexistence of mutualistic assemblages of generalists and their specialized variants.

     
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  3. Abstract

    The fate of diatoms in future acidified oceans could have dramatic implications on marine ecosystems, because they account for ~40% of marine primary production. Here, we quantify resilience ofThalassiosira pseudonanain mid-20th century (300 ppm CO2) and future (1000 ppm CO2) conditions that cause ocean acidification, using a stress test that probes its ability to recover from incrementally higher amount of low-dose ultraviolet A (UVA) and B (UVB) radiation and re-initiate growth in day–night cycles, limited by nitrogen. While all cultures eventually collapse, those growing at 300 ppm CO2succumb sooner. The underlying mechanism for collapse appears to be a system failure resulting from “loss of relational resilience,” that is, inability to adopt physiological states matched to N-availability and phase of the diurnal cycle. Importantly, under elevated CO2conditions diatoms sustain relational resilience over a longer timeframe, demonstrating increased resilience to future acidified ocean conditions. This stress test framework can be extended to evaluate and predict how various climate change associated stressors may impact microbial community resilience.

     
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