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Most of the Shewanella species contain two periplasmic nitrate reductases (NAP-α and NAP-β), which is a unique feature of this genus. In the present study, the physiological function and evolutionary relationship of the two NAP systems were studied in the deep-sea bacterium Shewanella piezotolerans WP3. Both of the WP3 nap gene clusters: nap-α (napD1A1B1C) and nap-β (napD2A2B2) were shown to be involved in nitrate respiration. Phylogenetic analyses suggest that NAP-β originated earlier than NAP-α. Tetraheme cytochromes NapC and CymA were found to be the major electron deliver proteins, and CymA also served as a sole electron transporter towards nitrite reductase. Interestingly, a ΔnapA2 mutant with the single functional NAP-α system showed better growth than the wild-type strain, when grown in nitrate medium, and it had a selective advantage to the wild-type strain. On the basis of these results, we proposed the evolution direction of nitrate respiration system in Shewanella: from a single NAP-β to NAP-β and NAP-α both, followed by the evolution to a single NAP-α. Moreover, the data presented here will be very useful for the designed engineering of Shewanella for more efficient respiring capabilities for environmental bioremediation.

Physiological and evolutionary studies of NAP systems in Shewanella piezotolerans WP3