Stress response of a freshwater clam along an abiotic gradient: too much oxygen may limit distribution

Abstract

Summary1. Distribution and abundance patterns are influenced by cellular responses to abiotic stressors. 2. The freshwater clam Sphaerium sp. inhabits swamp/stream systems in Uganda, in which dissolved O 2 (DO), pH and water transparency form ecotonal gradients along tributary streams. Along a swamp/stream transect, clam abundance was negatively related to DO, pH and transparency; clams were most abundant in the hypoxic/acidic swamp, less abundant in the ecotone, and absent from stream sites (neutral pH and higher DO). 3. We tested the hypothesis that individuals living in low abundance at the distribution edge have increased stress by assessing cellular-level stress indicators in clams from four sites: dense swamp interior (reference site), swamp margin, ecotone and stream. Compared with swamp interior clams, stream clams had decreased RNA : DNA ratio (decreased protein synthesis and growth) and increased DNA and RNA oxidation (free radical damage). Of seven stress proteins related to general damage and free radical detoxification, expression of nearly all were higher in margin and ecotone clams than in swamp interior or stream clams. 4. This pattern, which includes the first measurement of DNA and RNA oxidation in a natural population, demonstrates that stress increases along the transect, inversely to clam abundance. Additionally, this pattern is consistent with free radical stress, which suggests that inhabiting swamp conditions minimizes oxidative damage in this species.

Hydrogen Sulfide Induces Oxidative Damage to RNA and DNA in a Sulfide‐Tolerant Marine Invertebrate

“…We found that steady state levels of RNA oxidation in G. dibranchiata increased significantly with in vitro and in vivo sulfide exposure. In all cases, RNA oxidation was greater than DNA oxidation, which is consistent with the findings of previous studies (Hofer et al 2005, 2006; Joyner-Matos et al 2007). Interestingly, we also found that RNA oxidation was correlated with DNA oxidation in coelomocytes but not in the body wall tissue.…”

“…In the only measurement of 8-oxoGuo in a wild population of animals to date, there was a positive correlation between environmental dissolved O 2 concentration and RNA oxidation in a hypoxia-tolerant bivalve (Joyner-Matos et al 2007). RNA oxidation has otherwise not been extensively studied outside of its key role in Alzheimer’s disease (e.g., Nunomura et al 1999) and Parkinson’s disease (e.g., Zhang et al 1999) and its tendency to increase with age in mammals (Hofer et al 2005, 2006).…”

“…Samples of 100–200 mg of homogenized coelomocytes or 40–60 mg of homogenized body wall were processed with a method designed for vertebrate tissue (Hofer et al 2006) and optimized for invertebrate tissues (Joyner-Matos et al 2007). Briefly, RNA and DNA were simultaneously extracted from the homogenates by using guanidine thiocyanate and phenol/chloroform at neutral pH, after which nucleic acids were hydrolyzed with nuclease P 1 and alkaline phosphatase.…”

From molecules to living systems: historical and contemporary issues in oxidative stress and antioxidant ecology

“…For example, marine environments vary widely in thermal characteristics, partial pressure of oxygen, degree of pollution and light environment, all of which can influence the degree of oxidative insult experienced by an individual, and many marine organisms adjust their AO systems in response to this environmental variability to maintain a stable redox state (reviewed in Lesser 2006; Buttemer, Adele & Costantini 2010). Furthermore, within species, population densities can vary with habitat and, at least in freshwater clams ( Sphaerium sp), some of this variation has been tied to OD; clams were most abundant and showed lower levels of nucleic acid damage in relatively more hypoxic environments (Joyner‐Matos et al. 2007).…”

Hypotaurine and sulfhydryl-containing antioxidants reduce H2S toxicity in erythrocytes from a marine invertebrate

“…However, sulfide may also have antioxidant properties: H 2 S can directly scavenge reactive oxygen and nitrogen species (Whiteman et al, 2004;Whiteman et al, 2005), and reduce lipid peroxidation in a mouse model of hepatic ischemiareperfusion injury (Jha et al, 2008). Nonetheless, oxidative stress is increased in at least some marine organisms during sulfide exposure (Abele-Oeschger and Oeschger, 1995;Joyner-Matos et al, 2007;Julian et al, 2005;Tapley, 1993), as well as in mammalian cells exposed to sulfide in vitro (Attene-Ramos et al, 2007;Eghbal et al, 2004). Furthermore, environmental conditions other than sulfide, in particular high concentrations of dissolved metals, may contribute to oxidative stress at hydrothermal vents (Bebianno et al, 2005).…”