The impact of elevated CO2 on Prochlorococcus and microbial interactions with ‘helper’ bacterium Alteromonas

Abstract

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.

Cross‐protection from hydrogen peroxide by helper microbes: the impacts on the cyanobacterium Prochlorococcus and other beneficiaries in marine communities

“…At the optimum temperature for growth, the dominant surface ecotypes of Prochlorococcus are able to survive exposures up to about 800 nM HOOH (Morris et al, 2011). And, during exposure to elevated CO 2 , Alteromonas strain EZ55 increases SOD expression and decreases catalase expression in co-cultures with Prochlorococcus (Hennon et al, 2017). And, during exposure to elevated CO 2 , Alteromonas strain EZ55 increases SOD expression and decreases catalase expression in co-cultures with Prochlorococcus (Hennon et al, 2017).…”

“…However, at lower or higher temperatures, their sensitivity to HOOH increases significantly, such that at 400 nM, they can only grow at or just below their temperature optimum (22-248C) (Ma et al, 2017). And, during exposure to elevated CO 2 , Alteromonas strain EZ55 increases SOD expression and decreases catalase expression in co-cultures with Prochlorococcus (Hennon et al, 2017). This indicates that ocean acidification may enhance HOOH production (via SOD) and diminish HOOH degradation (via catalase) by these helpers, a prospect supported by a measured sixfold decrease in the HOOH removal rates in the Alteromonas/Prochlorococcus co-cultures, relative to the unamended (present-day CO 2 ) controls.…”

Competition and Synergy BetweenProchlorococcusandSynechococcusUnder Ocean Acidification Conditions

“…While carbon availability is unlikely to limit photosynthetic rates in the open ocean, projected year 2100 CO 2 concentrations nevertheless stimulate growth rates in laboratory cultures of several important phytoplankton taxa (Feng et al , 2008, Fu et al , 2008, Hutchins et al , 2007, Lefebvre et al , 2012, Li et al , 2012, Sobrino et al , 2008, Spielmeyer & Pohnert, 2012, Sun et al , 2011, Tatters et al , 2013). Other experiments have shown phytoplankton growing slower at higher CO 2 (Iglesias-Rodriguez et al , 2008, Hoogstraten et al , 2012, Muller et al , 2012, Hennon et al , 2018), and in some cases different strains of the same species have opposite response to high CO 2 , even when tested side-by-side by a single researcher (Langer et al , 2009). These differential responses appear to have ecological consequences, as addition of CO 2 (and concomitant reduction of pH) to natural seawater communities induces substantial shifts in phytoplankton community composition (Tortell et al , 2002, Hare et al , 2007).…”

“…However, Prochlorococcus was the one exception to the rule of increased growth rate at high CO 2 amongst cyanobacteria (Fu et al , 2007a), and as a consequence the models of Dutkiewicz et al that considered both temperature increase and ocean acidification predicted that the competitive balance between these two groups would shift sufficiently over the coming century that Synechococcus would replace Prochlorococcus throughout its range, essentially leading to the worldwide elimination of Prochlorococcus ’ niche (Dutkiewicz et al, 2015). While this remarkable conclusion was based on a single published experiment with a single cultured strain of each genus (Fu et al, 2007a), subsequent experiments have confirmed that gene expression of the “helper” heterotrophic bacteria that it depends on to tolerate ubiquitous oxidative stress exposure (Morris et al , 2011, Hennon et al, 2018).…”

“…Because understanding how critical taxa like Prochlorococcus will fare under future CO 2 conditions is key to our ability to predict how anthropogenic changes will impact the biogeochemistry and biodiversity of future oceans, we sought to increase our understanding of how ocean acidification might influence the interaction between Prochlorococcus and Synechococcus . First, we measured the GRR of several different isolates from each genus, including several well-characterized ecotypes of each, to determine if the differential responses previously reported (Fu et al , 2007b, Hennon et al, 2018) are representative. Second, we conducted direct, head-to-head competition experiments with Prochlorococcus and Synechococcus in co-culture to determine if predictions made from unialgal cultures reflected behavior in mixed communities.…”