Identification and characterization of carboxyl esterases of gill chamber-associated microbiota in the deep-sea shrimp rimicaris exoculata by using functional metagenomics

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Authors

Alcaide, María
Tchigvintsev, Anatoli
Martinez-Martinez, Monica
Popovic, Ana
Reva, Oleg N.
Lafraya, Alvaro
Bargiela, Rafael
Nechitaylo, Taras Y.
Matesanz, Ruth
Cambon-Bonavita, Marie-Ann

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American Society for Microbiology

Abstract

The shrimp Rimicaris exoculata dominates the fauna in deep-sea hydrothermal vent sites along the Mid-Atlantic Ridge (depth, 2,320 m). Here, we identified and biochemically characterized three carboxyl esterases from microbial communities inhabiting the R. exoculata gill that were isolated by naive screens of a gill chamber metagenomic library. These proteins exhibit low to moderate identity to known esterase sequences (<52%) and to each other (11.9 to 63.7%) and appear to have originated from unknown species or from genera of Proteobacteria related to Thiothrix/Leucothrix (MGS-RG1/RG2) and to the Rhodobacteraceae group (MGS-RG3). A library of 131 esters and 31 additional esterase/lipase preparations was used to evaluate the activity profiles of these enzymes. All 3 of these enzymes had greater esterase than lipase activity and exhibited specific activities with ester substrates (<356Umg 1) in the range of similar enzymes. MGS-RG3 was inhibited by salts and pressure and had a low optimal temperature (30°C), and its substrate profile clustered within a group of low-activity and substrate-restricted marine enzymes. In contrast, MGS-RG1 and MGS-RG2 were most active at 45 to 50°C and were salt activated and barotolerant. They also exhibited wider substrate profiles that were close to those of highly active promiscuous enzymes from a marine hydrothermal vent (MGS-RG2) and from a cold brackish lake (MGS-RG1). The data presented are discussed in the context of promoting the examination of enzyme activities of taxa found in habitats that have been neglected for enzyme prospecting; the enzymes found in these taxa may reflect distinct habitat-specific adaptations and may constitute new sources of rare reaction specificities.

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Rimicaris exoculata, Deep-sea shrimp, Metagenomics, Microorganisms, Enzyme activities

Sustainable Development Goals

Citation

Alcaide M, Tchigvintsev A, Martínez-Martínez M, Popovic A, Reva ON, Lafraya Á, Bargiela R, Nechitaylo TY, Matesanz R, Cambon-Bonavita M-A, Jebbar M, Yakimov MM, Savchenko A, Golyshina OV, Yakunin AF, Golyshin PN, Ferrer M, MAMBA Consortium. 2015. Identification and characterization of carboxyl esterases of gill chamber-associated microbiota in the deep-sea shrimp Rimicaris exoculata by using functional metagenomics. Applied and Environmental Microbiology 81:2125–2136. DOI: 10.1128/AEM.03387-14.