Temperature sensitivities of cytosolic malate dehydrogenases from native and invasive species of marine mussels (genusMytilus):sequence-function linkages and correlations with biogeographic distribution

Abstract

Coastal marine ecosystems are highly vulnerable to anthropogenically introduced invasive species, in part because movement of organisms between diverse and widely separated habitats can occur rapidly. High rates of translocation, most notably via the ballast water of ocean-going ships (Carlton and Geller, 1993), allow potential invaders repeated opportunities to colonize coastal habitats. Indeed, the result of such continual introductions over the past century has been a rapid increase in the number of successful colonizations by coastal and estuarine species (Cohen and Carlton, 1998). Clearly, however, not all species introduced into novel habitats colonize successfully, and a number of generalizations have been put forward to explain why certain invaders are able to compete successfully against aboriginal species (Kolar and Lodge, 2001;Lodge, 1993). These include high dispersal rates, phenotypic plasticity and pre-existing physiological suitability for the invaded habitat. Here, we explore whether biochemical adaptation to temperature potentially may play a role in invasion success, by comparing temperature sensitivity of the enzyme cytosolic malate dehydrogenase (cMDH) from three mussel congeners. Two of these mussels, Mytilus trossulus and M. californianus, are native to the west coast of North America and the third, M. galloprovincialis, is a species introduced there from the Mediterranean Sea.Mytilus trossulus and M. galloprovincialis are members of To test the effects of individual substitutions on kinetic properties, we used site-directed mutagenesis to create recombinant cMDHs. Recombinant wild-type M. trossulus cMDH (rWT) has high K m NADH compared with mutants incorporating the non-conservative substitutions found in M. californianus and M. galloprovincialis -V114H and V114N, respectively -demonstrating that these mutations are responsible for the differences found in substrate affinity. Turnover number (k cat ) is also higher in rWT compared with the two mutants, consistent with cold adaptation in the M. trossulus ortholog. Conversely, rWT and V114H appear more thermostable than V114N. Based on a comparison of K m NADH and k cat values among the orthologs, we propose that immersion temperatures are of greater selective importance in adapting kinetic properties than the more extreme temperatures that occur during emersion. The relative warm adaptation of M. galloprovincialis cMDH may be one of a suite of physiological characters that enhance the competitive ability of this invasive species in warm habitats.

Patterns and processes of compositional change in a California epibenthic community

“…increased anthropogenic transport of nonnatives in driving this pattern (e.g. Stachowicz et al 2002, Fields et al 2006, Chown et al 2007, Scheibling & Gagnon 2009, Sorte et al 2010a, Willis et al 2010. There is recent evidence that phenologies of nonnative species have shifted concurrently with global increases in air and ocean temperatures (IPCC 2007a): events such as flowering (Willis et al 2010) and recruitment (Stachowicz et al 2002) are now occurring earlier in the year, in a direction that could give non-natives an advantage via priority effects (see Shulman et al 1983) if natives do not respond similarly.…”

Latitudinal differences in Mytilus californianus thermal physiology

“…Preliminary data showed the possibility of differences in cMDH kinetic properties (Michaelis-Menten constant for cofactor NADH, K m NADH ) between mussels collected in this study as well (data not shown). Therefore, we investigated the possibility of a mutation in the cMDH genes at codon 114 (Fields et al 2006) that could underlie any potential differences. Codon 114 is known to differ between the 2 blue mussel congeners and M. californianus in a nonconservative amino acid substitution that is responsible for the differences found in substrate affinity (Fields et al 2006).…”

“…Therefore, we investigated the possibility of a mutation in the cMDH genes at codon 114 (Fields et al 2006) that could underlie any potential differences. Codon 114 is known to differ between the 2 blue mussel congeners and M. californianus in a nonconservative amino acid substitution that is responsible for the differences found in substrate affinity (Fields et al 2006).We dissected a small piece of foot tissue from the same 10 acclimated mussels per site that were used for the enzyme activities. Genomic DNA was ex tracted from each sample using a NucleoSpin DNA extraction kit (BD Biosciences).…”

Proteomic and metabolomic analysis on the toxicological effects of As (III) and As (V) in juvenile mussel Mytilus galloprovincialis

“…However, these identified proteomic responses in As (V)-exposed mussel samples were completely different from those of As (III)-exposed group. Cytosolic malate dehydrogenase (cMDH) plays an important role in energy metabolism (Dahlhoff and Somero, 1993;Fields et al, 2006). The up-regulated cMDH in As (V)-exposed samples indicated that the energy metabolism was disturbed by As (V) in juvenile mussel.…”