Prochlorococcus is a globally important marine cyanobacterium that lacks the gene catalase and relies on 'helper' bacteria such as Alteromonas to remove reactive oxygen species. Increasing atmospheric CO decreases the need for carbon concentrating mechanisms and photorespiration in phytoplankton, potentially altering their metabolism and microbial interactions even when carbon is not limiting growth. Here, Prochlorococcus (VOL4, MIT9312) was co-cultured with Alteromonas (strain EZ55) under ambient (400 p.p.m.) and elevated CO (800 p.p.m.). Under elevated CO, Prochlorococcus had a significantly longer lag phase and greater apparent die-offs after transfers suggesting an increase in oxidative stress. Whole-transcriptome analysis of Prochlorococcus revealed decreased expression of the carbon fixation operon, including carboxysome subunits, corresponding with significantly fewer carboxysome structures observed by electron microscopy. Prochlorococcus co-culture responsive gene 1 had significantly increased expression in elevated CO, potentially indicating a shift in the microbial interaction. Transcriptome analysis of Alteromonas in co-culture with Prochlorococcus revealed decreased expression of the catalase gene, known to be critical in relieving oxidative stress in Prochlorococcus by removing hydrogen peroxide. The decrease in catalase gene expression was corroborated by a significant ~6-fold decrease in removal rates of hydrogen peroxide from co-cultures. These data suggest Prochlorococcus may be more vulnerable to oxidative stress under elevated CO in part from a decrease in ecosystem services provided by heterotrophs like Alteromonas. This work highlights the importance of considering microbial interactions in the context of a changing ocean.The ISME Journal advance online publication, 31 October 2017; doi:10.1038/ismej.2017.189.

Atmospheric nitrogen (N) deposition has increased dramatically since preindustrial times and continues to increase across many regions of the Earth. In temperate forests, this agent of global change has increased soil carbon (C) storage, but the mechanisms underlying this response are not understood. One long‐standing hypothesis proposed to explain the accumulation of soil C proposes that higher inorganic N availability may suppress both the activity and abundance of fungi that decay lignin and other polyphenols in soil. In field studies, elevated rates of N deposition have reduced the activity of enzymes mediating lignin decay, but a decline in the abundance of lignolytic fungi has not been definitively documented to date. Here, we tested the hypothesis that elevated rates of anthropogenic N deposition reduce the abundance of lignolytic fungi. We conducted a field experiment in which we compared fungal communities colonizing low‐lignin, high‐lignin, and wood substrates in a northern hardwood forest that is part of a long‐term N deposition experiment. We reasoned that if lignolytic fungi decline under experimental N deposition, this effect should be most evident among fungi colonizing high‐lignin and wood substrates. Using molecular approaches, we provide evidence that anthropogenic N deposition reduces the relative abundance of lignolytic fungi on both wood and a high‐lignin substrate. Furthermore, experimental N deposition increased total fungal abundance on a low‐lignin substrate, reduced fungal abundance on wood, and had no significant effect on fungal abundance on a high‐lignin substrate. We simultaneously examined these responses in the surrounding soil and forest floor, in which we did not observe significant reductions in the relative abundance of lignolytic fungi or in the size of the fungal community; however, we did detect a change in community composition in the forest floor that appears to be driven by a shift away from lignolytic fungi and towards cellulolytic fungi. Our results provide direct evidence that reductions in the abundance of lignolytic fungi are part of the mechanism by which anthropogenic N deposition increases soil C storage.

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Terrestrial ecosystems in the Northern Hemisphere are a globally important sink for anthropogenic CO 2 in the Earth's atmosphere, slowing its accumulation as well as the pace of climate warming. With the use of a long-term field experiment (ca. 20 yr), we show that the expression of fungal class II peroxidase genes, which encode enzymes mediating the rate-limiting step of organic matter decay, are significantly downregulated (À60 to À80%) because of increases in anthropogenic N deposition; this response was consistent with a decline in extracellular peroxidase enzyme activity in soil, the slowing of organic-matter decay, and greater soil C storage. The reduction in peroxidase expression we document here occurred in the absence of a compositional shift in metabolically active fungi, indicating that an overall reduction in peroxidase expression underlies the slowing of decay and increases in soil C storage. This molecular mechanism has global implications for soil C storage and should be represented in coupled climate-biogeochemical models simulating the influence of enhanced terrestrial C storage on atmospheric CO 2 and the future climate of an N-enriched Earth.