Degradation of hydrogen peroxide at the ocean’s surface: the influence of the microbial community on the realized thermal niche of Prochlorococcus

Abstract

Prochlorococcus, the smallest and most abundant phytoplankter in the ocean, is highly sensitive to hydrogen peroxide (HOOH), and co-occurring heterotrophs such as Alteromonas facilitate the growth of Prochlorococcus by scavenging HOOH. Temperature is also a major influence on Prochlorococcus abundance and distribution in the ocean, and studies in other photosynthetic organisms have shown that HOOH and temperature extremes can act together as synergistic stressors. To address potential synergistic effects of temperature and HOOH on Prochlorococcus growth, high- and low-temperature-adapted representative strains were cultured at ecologically relevant concentrations under a range of HOOH concentrations and temperatures. Higher concentrations of HOOH severely diminished the permissive temperature range for growth of both Prochlorococcus strains. At the permissive temperatures, the growth rates of both Prochlorococcus strains decreased as a function of HOOH, and cold temperature increased susceptibility of photosystem II to HOOH-mediated damage. Serving as a proxy for the natural community, co-cultured heterotrophic bacteria increased the Prochlorococcus growth rate under these temperatures, and expanded the permissive range of temperature for growth. These studies indicate that in the ocean, the cross-protective function of the microbial community may confer a fitness increase for Prochlorococcus at its temperature extremes, especially near the ocean surface where oxidative stress is highest. This interaction may play a substantial role in defining the realized thermal niche and habitat range of Prochlorococcus with respect to latitude.The ISME Journal advance online publication, 31 October 2017; doi:10.1038/ismej.2017.182.

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

“…EZ55 -effectively dropped the HOOH to zero and facilitated the growth of all cultured ecotypes of Prochlorococcus. Consistently, we and others have found that treatment of the media with a chemical scavenger of HOOH, pyruvate, also promotes Prochlorococcus growth (Berube et al, 2015;Ma et al, 2017) [notably, additions of catalase to the medium do not support growth of Prochlorococcus; we have found that commercially available (e.g., bovine) catalase is unstable in seawater and becomes a net producer rather than consumer of ROS].…”

“…As described earlier, in our initial study identified 33 catalase-positive heterotrophic strains that could help Prochlorococcus grow on plates (Morris et al, 2008). Importantly, for many of the eukaryotes and for Prochlorococcus, the HOOH decay rates were not significant unless the cells were at much higher concentrations than they exist in the ocean (Petasne and Zika, 1997;Morris et al, 2011;Ma et al, 2017), and thus may not serve as significant sinks in situ. Other microbes shown to degrade HOOH in monoculture could potentially also serve as helpers.…”

“…Prokaryote examples include cyanobacteria such as Synechococcus and Prochlorococcus, and heterotrophs from multiple lineages including alpha and gamma Proteobacteria and the Flavobacteriaceae (Petasne and Zika, 1997;Morris et al, 2008;. Importantly, for many of the eukaryotes and for Prochlorococcus, the HOOH decay rates were not significant unless the cells were at much higher concentrations than they exist in the ocean (Petasne and Zika, 1997;Morris et al, 2011;Ma et al, 2017), and thus may not serve as significant sinks in situ. Alteromonas is not numerically abundant in the ocean (DeLong et al, 2006), but it is highly active (McCarren et al, 2010;Hunt et al, 2013) and is a very good scavenger of HOOH (Morris et al, 2011).…”

“…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). 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).…”

Thermal niches of specialized gut symbionts: the case of social bees

“…This 77 variability may impose divergent selection on symbiont thermal traits, with potential feedbacks 78 on the thermal tolerance of the hosts themselves. 79 We used common garden experiments (in vitro) to characterize symbiont thermal niches 80 with a culture collection of Snodgrassella and Gilliamella, two bacterial species that are 81 ubiquitous across honeybees and bumblebees [17]. Symbionts of these two bee lineages belong under 5% CO2, from 12-48 °C in increments of 4 °C.…”