Peroxisome Proliferation in Foraminifera Inhabiting the Chemocline: An Adaptation to Reactive Oxygen Species Exposure?¹

Abstract

Certain foraminiferal species are abundant within the chemocline of marine sediments. Ultrastructurally, most of these species possess numerous peroxisomes complexed with the endoplasmic reticulum; mitochondria are often interspersed among these complexes. In the Santa Barbara Basin, pore-water bathing Foraminifera and co-occurring sulfur-oxidizing microbial mats had micromolar levels of hydrogen peroxide, a reactive oxygen species that can be detrimental to biological membranes. Experimental results indicate that adenosine triphosphate concentrations are significantly higher in Foraminifera incubated in 16 μM H 2 O 2 than in specimens incubated in the absence of H 2 O 2 . New ultrastructural and experimental observations, together with published results, lead us to propose that foraminiferans can utilize oxygen derived from the breakdown of environmentally and metabolically produced H 2 O 2 . Such a capability could explain foraminiferal adaptation to certain chemically inhospitable environments; it would also force us to reassess the role of protists in biogeochemistry, especially with respect to hydrogen and iron. The ecology of these protists also appears to be tightly linked to the sulfur cycle. Finally, given that some Foraminifera bearing peroxisome-endoplasmic reticulum complexes belong to evolutionarily basal groups, an early acquisition of the capability to use environmental H 2 O 2 could have facilitated diversification of foraminiferans during the Neoproterozoic. KeywordsAnoxia; Beggiatoa; Blake Ridge; cold seep; hydrogen peroxide; hydrogen sulfide; microbial mat; Neoproterozoic; Santa Barbara Basin; Soledad BasinThe anoxic-oxic interface and associated reduction-oxidation (redox) zone are sites at which a great variety of biogeochemical reactions occur (e.g. Brune, Frenzel, and Cypionka 2000;Hulth et al. 2005;Preisler et al. 2007). In organic-rich sedimentary settings where the overlying waters are depleted of oxygen, redox gradients are particularly steep (e.g. Røy, Huettel, and Jørgensen 2005), and hydrogen sulfide can often reach considerable concentrations within one centimeter of the aerated sediment surface (e.g. Bernhard, (Tapley, Buettner, and Shick 1999). ROS are also formed as byproducts of normal metabolic reactions in most organisms (reviewed in Genestra 2007). Prolonged ROS exposure can seriously damage many biological molecules such as proteins, lipids, and nucleic acids, but cells normally have protective mechanisms by which to minimize the effect of such oxidative stress (e.g. Abele et al. 1998;Genestra 2007;Lesser 2006;Sigler et al. 1999). Because H 2 O 2 is an uncharged molecule, it is less reactive than most ROS and can cross biological membranes via diffusion and/or through channel proteins such as aquaporins ( This conversion typically is mediated by catalase, a metalloenzyme containing four porphyrin heme (iron) groups that react with hydrogen peroxide, which often appears as a crystalline core in peroxisomes (e.g. Masters and Crane 1995).Foraminifera (rhizarian protis...

Peroxisome diversity and evolution

“…Studies referring to peroxisomes in rhizarians are very scarce. Peroxisomes have been described as solitary organelles in several foraminiferan species, including those that inhabit the chemocline of marine sediments (Bernhard & Bowser 2008). In such anoxic environments, Foraminifera species might be associated with sulphur-oxidizing microbial mats, where micromolar levels of H 2 O 2 are observed.…”

Effects of natural and human-induced hypoxia on coastal benthos

“…These include the presence of bacterial symbionts (Bernhard, 2003) and sequestered chloroplasts (Bernhard and Bowser, 1999), as well as peroxisomes that facilitate the respiration of oxygen derived from the breakdown of hydrogen peroxide (Bernhard and Bowser, 2008). In addition, at least some hypoxia-tolerant species are able to respire nitrate (Risgaard-Petersen et al, 2006).…”

Is the meiofauna a good indicator for climate change and anthropogenic impacts?

“…Other likely mechanisms that allow foraminifera to live in hypoxic and anoxic sediments have been reviewed by Koho and Piña-Ochoa (2012). They include the presence of bacterial endosymbionts (e.g., Bernhard 2003), the sequestration of chloroplasts (Bernhard and Bowser 1999;Grzymski et al 2002), the proliferation of peroxisomes and mitochondria (Bernhard and Bowser 2008), and most notably, the respiration of stored nitrates (Risgaard-Petersen et al 2006;Piña-Ochoa et al 2010a, b). Denitrification as an alternative metabolic pathway, together with other physiological and ultrastructural adaptations, make foraminifera an important ecological group in oxygen-depleted environments (e.g., Woulds et al 2007;Gooday et al 2009a, b;Glock et al 2012;Koho and Piña-Ochoa 2012;Mallon et al 2012;Fontanier et al 2014).…”