38
3.2 Tolerance Mechanisms in Seaweeds to Heavy Metal
Toxicity
Seaweeds accumulate metals through a two-stage process that begins with a rapid
and reversible physicochemical adsorption on the algal surface, followed by a
slower, metabolically arranged intracellular uptake (Garnham et al. 1992). Therefore,
heavy metal concentration is generally dependent both on external factors (pH,
salinity, and complex inorganic and organic molecules) and on physicochemical
parameters that control metabolic rate (temperature, light, oxygen, and nutrients).
One clear effect of heavy metals on marine organisms, including seaweeds, is the
rapid formation of reactive oxygen species (ROS) through the Haber-Weiss reaction,
which is characterized by a heavy metal-catalyzed production of hydroxyl radicals
from hydrogen peroxide (Gledhill et al. 1997; Pinto et al. 2003) (Fig. 3.1). ROS are
directly produced by O 2 excitation and the subsequent formation of singlet oxygen, or
by the transfer of one, two, or three electrons to O 2 , which results in the formation of
superoxide radicals, hydrogen peroxide, or hydroxyl radicals, respectively. The production of ROS beyond the physiological tolerance range of an organism can negatively affect physiological maintenance due to oxidative damage to cellular constituents
such as DNA/RNA, proteins, and lipids (Vranová et al. 2002; Hung et al. 2005;
Contreras et al. 2009; Lovazzano et al. 2013) (Fig. 3.1). This overproduction can lead
to a state of oxidative stress, but a coordinated attenuation system can be activated by
the affected organism to eliminate ROS excess (Collén and Davison 1999; Sordet et al.
2014). To cope with heavy metal excess, several mechanisms exist in tolerant seaweed
species such as Scytosiphon spp. (Phaeophyceae) or Ulva spp. (Ulvophyceae), including the activation of an efficient ROS-scavenging system constituted by compounds
and enzymes, including catalase (CAT), ascorbate peroxidase (AP), peroxiredoxin
(PRX), and lipoxygenase, among others (Ratkevicius et al. 2003; Contreras et al.
2005; Contreras et al. 2010; Lovazzano et al. 2013) (Fig. 3.1). In contrast, species
sensitive to heavy metal excess have low activities of tolerance response enzymes,
which would explain the inability to flourish in heavy metal-enriched environments.
For example, activities of diverse antioxidant enzymes are lower in the sensitive species L. spicata than in the tolerant Scytosiphon lomentaria, and others as glutathione
peroxidase (GP) and dehydroascorbate reductase (DHAR) are completely inhibited
at higher copper concentrations (Contreras et al. 2009). Copper toxicity also induces
uncontrolled lipoperoxide accumulation in L. spicata, which leads to cell damage
and dysfunction.
Using proteomic analysis, a PRX was identified in Scytosiphon gracilis exposed
to copper excess (Contreras et al. 2010). PRXs belong to the thiol-dependent peroxidase family and are known to attenuate oxidative stress; reduce hydrogen peroxide,
alkyl hydroperoxides, and peroxynitrite; and modulate redox-dependent signaling
cascades (Dayer et al. 2008; Foyer and Noctor 2009; Tripathi et al. 2009; Dietz
2011). In algae, the protective function of PRXs is scarcely documented. For example, the prx gene, which presents homology with the 2-Cys PRX of higher plants
(Baier and Dietz 1997), was first identified in Porphyra purpurea (Bangiophyceae)
(Reith and Munholland 1993). By studying the responses to desiccation stress in
L. Contreras-Porcia et al.
3.2 Tolerance Mechanisms in Seaweeds to Heavy Metal
Toxicity
Seaweeds accumulate metals through a two-stage process that begins with a rapid
and reversible physicochemical adsorption on the algal surface, followed by a
slower, metabolically arranged intracellular uptake (Garnham et al. 1992). Therefore,
heavy metal concentration is generally dependent both on external factors (pH,
salinity, and complex inorganic and organic molecules) and on physicochemical
parameters that control metabolic rate (temperature, light, oxygen, and nutrients).
One clear effect of heavy metals on marine organisms, including seaweeds, is the
rapid formation of reactive oxygen species (ROS) through the Haber-Weiss reaction,
which is characterized by a heavy metal-catalyzed production of hydroxyl radicals
from hydrogen peroxide (Gledhill et al. 1997; Pinto et al. 2003) (Fig. 3.1). ROS are
directly produced by O 2 excitation and the subsequent formation of singlet oxygen, or
by the transfer of one, two, or three electrons to O 2 , which results in the formation of
superoxide radicals, hydrogen peroxide, or hydroxyl radicals, respectively. The production of ROS beyond the physiological tolerance range of an organism can negatively affect physiological maintenance due to oxidative damage to cellular constituents
such as DNA/RNA, proteins, and lipids (Vranová et al. 2002; Hung et al. 2005;
Contreras et al. 2009; Lovazzano et al. 2013) (Fig. 3.1). This overproduction can lead
to a state of oxidative stress, but a coordinated attenuation system can be activated by
the affected organism to eliminate ROS excess (Collén and Davison 1999; Sordet et al.
2014). To cope with heavy metal excess, several mechanisms exist in tolerant seaweed
species such as Scytosiphon spp. (Phaeophyceae) or Ulva spp. (Ulvophyceae), including the activation of an efficient ROS-scavenging system constituted by compounds
and enzymes, including catalase (CAT), ascorbate peroxidase (AP), peroxiredoxin
(PRX), and lipoxygenase, among others (Ratkevicius et al. 2003; Contreras et al.
2005; Contreras et al. 2010; Lovazzano et al. 2013) (Fig. 3.1). In contrast, species
sensitive to heavy metal excess have low activities of tolerance response enzymes,
which would explain the inability to flourish in heavy metal-enriched environments.
For example, activities of diverse antioxidant enzymes are lower in the sensitive species L. spicata than in the tolerant Scytosiphon lomentaria, and others as glutathione
peroxidase (GP) and dehydroascorbate reductase (DHAR) are completely inhibited
at higher copper concentrations (Contreras et al. 2009). Copper toxicity also induces
uncontrolled lipoperoxide accumulation in L. spicata, which leads to cell damage
and dysfunction.
Using proteomic analysis, a PRX was identified in Scytosiphon gracilis exposed
to copper excess (Contreras et al. 2010). PRXs belong to the thiol-dependent peroxidase family and are known to attenuate oxidative stress; reduce hydrogen peroxide,
alkyl hydroperoxides, and peroxynitrite; and modulate redox-dependent signaling
cascades (Dayer et al. 2008; Foyer and Noctor 2009; Tripathi et al. 2009; Dietz
2011). In algae, the protective function of PRXs is scarcely documented. For example, the prx gene, which presents homology with the 2-Cys PRX of higher plants
(Baier and Dietz 1997), was first identified in Porphyra purpurea (Bangiophyceae)
(Reith and Munholland 1993). By studying the responses to desiccation stress in
L. Contreras-Porcia et al.