Flatfishes colonised freshwater environments by acquisition of various DHA biosynthetic pathways

Abstract

The colonisation of freshwater environments by marine fishes has historically been considered a result of adaptation to low osmolality. However, most marine fishes cannot synthesise the physiologically indispensable fatty acid, docosahexaenoic acid (DHA), due to incomplete DHA biosynthetic pathways, which must be adapted to survive in freshwater environments where DHA is poor relative to marine environments. By analysing DHA biosynthetic pathways of one marine and three freshwater-dependent species from the flatfish family Achiridae, we revealed that functions of fatty acid metabolising enzymes have uniquely and independently evolved by multi-functionalisation or neofunctionalisation in each freshwater species, such that every functional combination of the enzymes has converged to generate complete and functional DHA biosynthetic pathways. Our results demonstrate the elaborate patchwork of fatty acid metabolism and the importance of acquiring DHA biosynthetic function in order for fish to cross the nutritional barrier at the mouth of rivers and colonise freshwater environments.

The evolutionary ecology of fatty‐acid variation: Implications for consumer adaptation and diversification

“…Individuals from range‐edge and range‐core populations also frequently differ in patterns of gene expression and metabolism (Rollins et al, 2015; Van Petegem et al, 2016). Recent studies suggest that metabolic traits may be also under strong selective pressure, particularly when the colonising consumer is faced with a novel resource environment, such as when marine consumers invade freshwater ecosystems (e.g., Ishikawa et al, 2019; Matsushita et al, 2020).…”

“…Specifically, local metabolic adaptation can culminate in shifts in network topologies, potentially opening new opportunities for evolutionary diversity (Badyaev, 2019b). Currently, this is unexplored in the context of fatty acid metabolism, but there is considerable potential to do so in light of the heterogeneity of FA within and amongst ecosystems (Figure 2), variation in genes related to fatty acid synthesis across consumers, the fitness relevance of FA acquisition, retention and synthesis traits and examples of key innovations facilitating consumer diversification (Ishikawa et al, 2019; Matsushita et al, 2020).…”

Influence of Dietary Lipids and Environmental Salinity on the n-3 Long-Chain Polyunsaturated Fatty Acids Biosynthesis Capacity of the Marine Teleost Solea senegalensis

“…While teleost Fads2 are often neo- and sub-functionalised enzymes [ 16 ], the multifunctionality of flatfish Fads2 is particularly remarkable. Indeed, the Δ6/Δ5/Δ4 desaturation abilities of the S. senegalensis Fads2 have also been reported in several flatfish species including Trinectes maculatus , Apionichthys finis and Hypoclinemus mentalis [ 44 ]. Interestingly, whereas the T. maculatus and A. finis Fads2 had Δ6 as their most prominent activity in yeast, the highest desaturase activity within the Δ6/Δ5/Δ4 Fads2 from S. senegalensis and H. mentalis was Δ4, raising the question of whether S. senegalensis possesses further fads2 -like genes that could also contribute to the Δ6 and Δ5 desaturations observed in our in vitro assays.…”

“…Interestingly, whereas the T. maculatus and A. finis Fads2 had Δ6 as their most prominent activity in yeast, the highest desaturase activity within the Δ6/Δ5/Δ4 Fads2 from S. senegalensis and H. mentalis was Δ4, raising the question of whether S. senegalensis possesses further fads2 -like genes that could also contribute to the Δ6 and Δ5 desaturations observed in our in vitro assays. This is actually the case with H. mentalis that, along the high Δ4 trifunctional Fads2 alluded to above (termed “Fads2b” by Matsushita et al [ 44 ]), has a second Fads2 ("Fads2a”) with ∆6 and ∆5 activities [ 44 ]. While the exact number of Fads2 in S. senegalensis remains to be elucidated, data collected from the present and other studies [ 21 , 43 ] allow us to establish that S. senegalensis has at least one Fads2 with ∆6 activity.…”

The evolutionary ecology of fatty-acid variation: implications for consumer adaptation and diversification

“…Specifically, local metabolic adaptation can culminate in shifts in network topologies, potentially opening new opportunities for evolutionary diversity (Badyaev, 2019b). Currently, this is unexplored in the context of fatty acid metabolism, but there is considerable potential to do so in light of the heterogeneity of FA within and amongst ecosystems (Figure 2), variation in genes related to fatty acid synthesis across consumers, the fitness relevance of FA acquisition, retention and synthesis traits and examples of key innovations facilitating consumer diversification (Ishikawa et al, 2019;Matsushita et al, 2020).…”