Major Effect of Hydrogen Peroxide on Bacterioplankton Metabolism in the Northeast Atlantic

Abstract

Reactive oxygen species such as hydrogen peroxide have the potential to alter metabolic rates of marine prokaryotes, ultimately impacting the cycling and bioavailability of nutrients and carbon. We studied the influence of H2O2 on prokaryotic heterotrophic production (PHP) and extracellular enzymatic activities (i.e., β-glucosidase [BGase], leucine aminopeptidase [LAPase] and alkaline phosphatase [APase]) in the subtropical Atlantic. With increasing concentrations of H2O2 in the range of 100–1000 nM, LAPase, APase and BGase were reduced by up to 11, 23 and 62%, respectively, in the different water layers. Incubation experiments with subsurface waters revealed a strong inhibition of all measured enzymatic activities upon H2O2 amendments in the range of 10–500 nM after 24 h. H2O2 additions also reduced prokaryotic heterotrophic production by 36–100% compared to the rapid increases in production rates occurring in the unamended controls. Our results indicate that oxidative stress caused by H2O2 affects prokaryotic growth and hydrolysis of specific components of the organic matter pool. Thus, we suggest that oxidative stress may have important consequences on marine carbon and energy fluxes.

Hydrogen peroxide detoxification is a key mechanism for growth of ammonia-oxidizing archaea

“…In this setting, these AOA perform nitrification (32,33), often under oligotrophic conditions (ammonia concentrations <5 nM) (21). In these environments, the H 2 O 2 concentration is also extremely low (i.e., in the 5-10-nM range) (34). Therefore, over evolutionary time, many autotrophic AOA may have dispensed with their burden of ROS-detoxification genes (such as those encoding catalase) to streamline their genome for efficient use of rare resources.…”

“…There may be H 2 O 2 -tolerant AOA ecotypes featuring traits adapted to distinct habitats. For example, in the epipelagic zone, photochemical reactions can boost H 2 O 2 concentrations by orders of magnitude (i.e., up to ∼0.4 μM) (20,34). Furthermore, single-cell genome analysis of epipelagic AOA ecotypes has revealed that they do harbor putative catalase genes (35).…”

Marine Photochemistry of Organic Matter

“…Factors resulting in a negative or mixed effect include photochemical production of inhibitory substances such as hydrogen peroxide (Angel et al, 1999;Baltar et al, 2013;Farjalla et al, 2001;Gjessing and Källqvist, 1991;Kaiser and Sulzberger, 2004;Leunert et al, 2014;Lund and Hongve, 1994;Morris et al, 2011;Scully et al, 2003a;Tranvik and Kokalj, 1998;Weinbauer and Suttle, 1999), release of toxic metals (e.g., Pb, Cu, Ni, Cd, and Hg) from DOM complexes (Haverstock et al, 2012;Tonietto et al, 2011;Winch and Lean, 2005), photolysis of DOM to form substances that are both biologically and photochemically refractory (Kieber, 2000;Stubbins et al, 2010), deactivation of enzymes (Scully et al, 2003b;Vähätalo et al, 2003), changes in the BGE (Abboudi et al, 2008;McCallister et al, 2005;Mopper and Kieber, 2002;Pullin et al, 2004;Smith and Benner, 2005), changes in microbial populations (i.e., community structure) in response to photoproduced substrates or toxic substances (Abboudi et al, 2008;Calza et al, 2008;Lønborg et al, 2013;Piccini et al, 2009), and prior photochemical history, i.e., photon dose-related bleaching (Reader and Miller, 2014). In addition to the above factors, a negative or mixed effect on biological activity can result from reactions of biologically produced ROS, e.g., H 2 O 2 (Palenik and Morel, 1990;Diaz et al, 2013) with photochemically produced reduced metals, e.g., Fe(II), Mn(II), and Cu(I) (Barbeau, 2006;Brinkmann et al, 2003;…”

“…In contrast, studies with long-term incubation times (e.g., days to weeks or longer) often showed an initial lag period (with no or negative effect) followed by a positive effect on microbial activity (Anesio et al, 2005;Biddanda and Cotner, 2003;Judd et al, 2007;McCallister et al, 2005;Obernosterer and Benner, 2004;Pullin et al, 2004;Smith and Benner, 2005) or enzymatic activity (Vähätalo et al, 2003). The initial lag (or negative effect) may have been due to the photoproduction of inhibitory substances such as ROS or toxins (Anesio et al, 1999(Anesio et al, , 2005Angel et al, 1999;Baltar et al, 2013;Calza et al, 2008;Diamond, 2003;Farjalla et al, 2001;Goldstone et al, 2002;Kaiser and Sulzberger, 2004;Leunert et al, 2014;Lund and Hongve, 1994;Morris et al, 2011;Scully et al, 2003b;Tranvik and Kokalj, 1998;Weinbauer and Suttle, 1999) that decayed over time (Anesio et al, 2005;Goldstone et al, 2002), or induced a change in the microbial community structure to species less affected by photoproduced toxins and/or better adapted to utilizing photoproduced products (Abboudi et al, 2008;Judd et al, 2007;Langenheder et al, 2006;Pérez and Sommaruga, 2007;Piccini et al, 2009;Pullin et al, 2004;Vähätalo et al, 2003). Alternatively, the lag period may be the time needed for microbes to biodegrade photoaltered high molecular weight (HMW) DOM to LMW membrane-transp...…”

Dynamics of hydrogen peroxide in a coral reef: Sources and sinks

“…[4] At a first glance the intracellular levels of H 2 O 2 and its dynamics in seawater have little in common. Yet, since H 2 O 2 is membrane permeable, its presence in seawater can cause deleterious effects to marine organisms such as bacteria and phytoplankton [Baltar et al, 2013;Morris et al, 2011]. On the other hand, marine microbes can influence H 2 O 2 dynamics in seawater by producing and degrading H 2 O 2 [Hansard et al, 2010;Palenik and Morel, 1988;Rose et al, 2010;Wong et al, 2003].…”