The Capability of Utilizing Abiotic Enantiomers of Amino Acids by Halomonas sp. LMO_D1 Derived From the Mariana Trench

Abstract

D-amino acids (D-AAs) have been produced both in organisms and in environments via biotic or abiotic processes. However, the existence of these organic materials and associated microbial degradation activity has not been previously investigated in subduction zones where tectonic activities result in the release of hydrothermal organic matter. Here, we isolated the bacterium Halomonas sp. LMO_D1 from a sample obtained from the Mariana trench, and we determined that this isolate utilized 13 different D-AAs (D-Ala, D-Glu, D-Asp, D-Ser, D-Leu, D-Val, D-Tyr, D-Gln, D-Asn, D-Pro, D-Arg, D-Phe, and D-Ile) in the laboratory and could grow on D-AAs under high hydrostatic pressure (HHP). Moreover, the metabolism of L-AAs was more severely impaired under HHP conditions compared with that of their enantiomers. The essential function gene (Chr_2344) required for D-AA catabolism in strain LMO_D1 was identified and confirmed according to the fosmid library method used on the D-AAs plate. The encoded enzyme of this gene (DAADH_2344) was identified as D-amino acid dehydrogenase (DAADH), and this gene product supports the catabolism of a broad range of D-AAs. The ubiquitous distribution of DAADHs within the Mariana Trench sediments suggests that microorganisms that utilize D-AAs are common within these sediments. Our findings provide novel insights into the microbial potential for utilizing abiotic enantiomers of amino acids within the subduction zone of the Mariana trench under HHP, and our results provide an instructive significance for understanding these abiotic enantiomers and allow for insights regarding how organisms within extraterrestrial HHP environments can potentially cope with toxic D-AAs.

Prophage enhances the ability of deep-sea bacterium Shewanella psychrophila WP2 to utilize D-amino acid

“…D-AAs are among the most important components of RDOM, which are widely present in the deep sea and has a higher concentration in marine sediments than in seawater ( 14 ). At present, a variety of deep-sea microorganisms that can utilize D-AAs have been isolated ( 18 , 20 ), and the bioavailability of D-AAs in the deep ocean has been shown to be equal to or even higher than that of L-AAs ( 20 , 40 ); thus, D-AAs are an important source of nutrients for benthic microbes. In this study, we found that the deep-sea sediment-derived Shewanella strain WP2 can utilize D-Glu, D-Ala, and D-Ser as a single nitrogen source for growth.…”

“…Although D-AAs are normally considered RDOM, they can be utilized by some microorganisms as nutrient sources ( 4 , 15 ). Recently, many D-AA-utilizing microorganisms have been found in diverse habitats, including soils, limnological waters, marine sediments, and seawater ( 16 – 18 ). For samples from the surface seawater and sediments (depth <356 m) of Kongsfjorden, bacterial strains belonging to 12 families and 3 phyla were enriched in culture with D-AAs as the sole nitrogen source.…”

“…From Sagami Bay sediments (from 800 m to 1,500 m), 28 strains were isolated, most of which belonged to Alphaproteobacteria ( 20 ). By using sediment from the Mariana Trench, microbes belonging to eight bacterial genera and other unidentified genera were enriched when the sample was supplied with D-AAs as the sole carbon source, and the genus Halomonas was dominant in the enriched sample ( 18 ). Interestingly, Nautella sp.…”

“…The metabolism of Halomonas sp. LMO_D1, which was isolated from Mariana Trench sediments with a water depth of 8,636 m, was more severely impaired with L-AAs under high hydrostatic pressure compared to their enantiomers ( 18 ). Furthermore, the uptake ratio of D-Asp/L-aspartate (L-Asp) by bacterioplankton in the water column increased with depth (the value reached ~1 at 1,000 m), which indicated that the utilization efficiency of D-Asp by mesophyll bacteria was almost as effective as that of L-Asp ( 21 ).…”

Comparison of prokaryotes between Mount Everest and the Mariana Trench

“…Notably, for D-amino acid (D-AA) metabolism, the catabolic capacities for nine D-AAs, including two typical D-AAs in bacterial cell walls (i.e., D-Ala, D-Glu) and seven non-canonical D-AAs (i.e., D-Gln, D-Ser, D-Thr, D-Arg, D-Pro, D-Phe and D-Cys), were found in MAGs from both ME and MT. Among them, dadA, the typical gene for a broad-spectrum D-AA dehydrogenase in D-AA catabolism [62], was abundant and found in 445 (of 1176) MAGs (59% in ME and 35% in MT). Almost all identified class-level clades (81/84) contain at least one D-AA metabolic gene(s) (Fig.…”