Abstract

Selenium is an important trace element that occurs in proteins in the form of selenocysteine (Sec) and in tRNAs in the form of selenouridine. Recent large-scale metagenomics projects provide an opportunity for understanding global trends in trace element utilization. Herein, we characterized the selenoproteome of the microbial marine community derived from the Global Ocean Sampling (GOS) expedition. More than 3,600 selenoprotein gene sequences belonging to 58 protein families were detected, including sequences representing 7 newly identified selenoprotein families, such as homologs of ferredoxin–thioredoxin reductase and serine protease. In addition, a new eukaryotic selenoprotein family, thiol reductase GILT, was identified. Most GOS selenoprotein families originated from Cys-containing thiol oxidoreductases. In both Pacific and Atlantic microbial communities, SelW-like and SelD were the most widespread selenoproteins. Geographic location had little influence on Sec utilization as measured by selenoprotein variety and the number of selenoprotein genes detected; however, both higher temperature and marine (as opposed to freshwater and other aquatic) environment were associated with increased use of this amino acid. Selenoproteins were also detected with preference for either environment. We identified novel fusion forms of several selenoproteins that highlight redox activities of these proteins. Almost half of Cys-containing SelDs were fused with NADH dehydrogenase, whereas such SelD forms were rare in terrestrial organisms. The selenouridine utilization trait was also analyzed and showed an independent evolutionary relationship with Sec utilization. Overall, our study provides insights into global trends in microbial selenium utilization in marine environments.

Highlights

  • Selenium (Se) is an essential trace element that exerts a number of health benefits yet is required only in small amounts [1,2,3]

  • The translation of selenoprotein mRNAs requires both a cis-acting selenocysteine insertion sequence (SECIS) element, which is a hairpin structure residing in 39-untranslated regions (39-UTRs) of selenoprotein mRNAs in eukaryota and archaea, or immediately downstream of Sec-encoding UGA codons in bacteria [7,13,14,15,16], and several trans-acting factors dedicated to Sec incorporation [7,17]

  • We describe a comprehensive analysis of the selenoproteome of the microbial marine community derived from the Global Ocean Sampling (GOS) expedition

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Summary

Introduction

Selenium (Se) is an essential trace element that exerts a number of health benefits yet is required only in small amounts [1,2,3]. It is incorporated into selenoproteins, many of which are important antioxidant enzymes, in all three domains of life, and occurs in these proteins in the form of selenocysteine (Sec), the twenty-first amino acid in the genetic code [4,5,6]. The translation of selenoprotein mRNAs requires both a cis-acting selenocysteine insertion sequence (SECIS) element, which is a hairpin structure residing in 39-untranslated regions (39-UTRs) of selenoprotein mRNAs in eukaryota and archaea, or immediately downstream of Sec-encoding UGA codons in bacteria [7,13,14,15,16], and several trans-acting factors dedicated to Sec incorporation [7,17]

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