ABSTRACT

Dimethylsulfoniopropionate (DMSP) is one of the most abundant organic sulfur compounds in the oceans, which is mainly degraded by bacteria through two pathways, a cleavage pathway and a demethylation pathway. Its volatile catabolites dimethyl sulfide (DMS) and methanethiol (MT) in these pathways play important roles in the global sulfur cycle and have potential influences on the global climate. Intense DMS/DMSP cycling occurs in the Arctic. However, little is known about the diversity of cultivable DMSP-catabolizing bacteria in the Arctic and how they catabolize DMSP. Here, we screened DMSP-catabolizing bacteria from Arctic samples and found that bacteria of four genera (Psychrobacter, Pseudoalteromonas, Alteromonas, and Vibrio) could grow with DMSP as the sole carbon source, among which Psychrobacter and Pseudoalteromonas are predominant. Four representative strains (Psychrobacter sp. K31L, Pseudoalteromonas sp. K222D, Alteromonas sp. K632G, and Vibrio sp. G41H) from different genera were selected to probe their DMSP catabolic pathways. All these strains produce DMS and MT simultaneously during their growth on DMSP, indicating that all strains likely possess the two DMSP catabolic pathways. On the basis of genomic and biochemical analyses, the DMSP catabolic pathways in these strains were proposed. Bioinformatic analysis indicated that most Psychrobacter and Vibrio bacteria have the potential to catabolize DMSP via the demethylation pathway and that only a small portion of Psychrobacter strains may catabolize DMSP via the cleavage pathway. This study provides novel insights into DMSP catabolism in marine bacteria.
IMPORTANCE Dimethylsulfoniopropionate (DMSP) is abundant in the oceans. The catabolism of DMSP is an important step of the global sulfur cycle. Although Gammaproteobacteria are widespread in the oceans, the contribution of Gammaproteobacteria in global DMSP catabolism is not fully understood. Here, we found that bacteria of four genera belonging to Gammaproteobacteria (Psychrobacter, Pseudoalteromonas, Alteromonas and Vibrio), which were isolated from Arctic samples, were able to grow on DMSP. The DMSP catabolic pathways of representative strains were proposed. Bioinformatic analysis indicates that most Psychrobacter and Vibrio bacteria have the potential to catabolize DMSP via the demethylation pathway and that only a small portion of Psychrobacter strains may catabolize DMSP via the cleavage pathway. Our results suggest that novel DMSP dethiomethylases/demethylases may exist in Pseudoalteromonas, Alteromonas, and Vibrio and that Gammaproteobacteria may be important participants in the marine environment, especially in polar DMSP cycling.

INTRODUCTION

Dimethylsulfoniopropionate (DMSP) is an abundant organic sulfur compound widespread in Earth’s oceans. It is mainly produced by marine phytoplankton and macroalgae (1, 2), such as coccolithophores, dinoflagellates, and diatoms (2, 3). It can also be produced by bacteria (3, 4), some corals (5), and a few angiosperms (6). DMSP is mainly catabolized by marine bacteria as an important carbon and/or sulfur source through the cleavage and/or the demethylation pathways (79). While converting a large fraction (50% to 90%) of DMSP to 3-methylmercaptopropionate (MMPA) and finally to methanethiol (MT) through the demethylation pathway (10), marine microorganisms also catabolize DMSP to dimethyl sulfide (DMS) and acrylate (acryloyl-CoA or 3-hydroxypropionate coenzyme A, 3HP-CoA) via the cleavage pathway (1114). DMS, mainly produced from the cleavage of DMSP, is one of the most important natural sources of sulfur emitted from the sea to the atmosphere (4). The oxidative products of DMS can act as cloud condensation nuclei (CCN), which affects the formation of cloud and thus the solar radiation reaching Earth’s surface (15, 16).
In the cleavage pathway, one DMSP CoA-transferase DddD (EC 2.8.3.x) (4), one DMSP-CoA ligase DddX (EC 6.2.1.x) (14), and seven isoenzymes of DMSP dethiomethylases (colloquial “DMSP lyases” EC 4.4.1.3), including DddL, DddP, DddQ, DddW, DddK, DddY and Alma1 (4, 17), have been reported. DddP and DddQ are the most abundant bacterial DMSP dethiomethylases in the Global Ocean Sampling database (18). DddD degrades DMSP into DMS and 3HP-CoA, DddX degrades DMSP into DMS and acryloyl-CoA, and the DMSP dethiomethylases cleave DMSP to generate DMS and acrylate. 3HP-CoA is further catabolized by ethanol dehydrogenase DddA/DddB (EC 1.1.1.x) and acetaldehyde dehydrogenase DddC (EC 1.2.1.10) to produce acetyl-CoA, which enters into the tricarboxylic acid cycle for further catabolism (4, 13, 19). Acryloyl-CoA is further catabolized by acryloyl-CoA reductase AcuI (EC 1.3.1.84) to propionyl-CoA (14). Two pathways for acrylate catabolism have been reported in bacteria, the AcuN-AcuK (EC 2.8.3.x and EC 4.2.1.x) pathway and the PrpE-AcuI (EC 6.3.1.x and EC 1.3.1.84) pathway (20, 21). In the DMSP demethylation pathway, DMSP is first demethylated by DMSP demethylase DmdA (EC 2.1.1.269), and then successively catabolized into MT by CoA ligase DmdB (EC 6.2.1.x), MMPA-CoA dehydrogenase DmdC (EC 1.1.1.x) and methylthioacryloyl-CoA (MTA-CoA) hydratase DmdD/AcuH (EC 4.2.1.x) (10). DmdA, the key enzyme in this pathway, has been reported to be prevalent in the marine Roseobacter clade (MRC) and SAR11 clade, which are considered the main bacterial groups for DMSP catabolism in the oceans (22).
Current studies of DMSP catabolism mainly focus on the oceans in low and mid latitudes (23). However, polar oceans usually contain more DMSP than oceans in low or mid latitudes and contribute significantly to the global oceanic DMS sea-air flux (2426). Especially, in the summertime, the pan-Arctic DMS emission from ice-free waters increased at a mean rate of 33% decade−1 in the north of 70°N between 1998 and 2016 (27). Therefore, intense DMS/DMSP cycling occurs in the Arctic (28). DMSP concentrations in the Arctic generally ranged from 2–70 nM (26). Bioinformatic analysis indicated that 40–65% of bacterial cells in the Arctic seawater could absorb soluble DMSP, with the majority of which being Gammaproteobacteria and non-Roseobacter Alphaproteobacteria, and different areas of the Arctic contain relatively unique microbial communities (29). However, only a few cultivable polar bacteria that can utilize DMSP have been reported. Zeng et al. reported 13 bacterial strains isolated from the Arctic Kongsfjorden seawater using oligotrophic plates containing DMSP, which all belonged to Gammaproteobacteria (30). In addition, several strains isolated from polar oceans, including Pseudomonas sp. BSw22131, Sulfitobacter sp. BSw21498, and Rhodococcus sp. NJ-530, have been reported to be able to grow with DMSP as the sole carbon source (31, 32). Among them, only strain Rhodococcus sp. NJ-530 was shown to be able to degrade DMSP into DMS (32). Studies based on gene library construction and analysis showed that the gene dmdA was prevalent in bipolar regions, dddP was found in coastal seawaters of Maxwell Bay, and a few dddL homologs were detected in the surface seawater of the Arctic (30, 33). In polar bacteria, the gene dmdA was found in Pseudoalteromonas, Pseudomonas, Glaciecola, and Roseobacter (31), the dddL gene was found in Sulfitobacter (31), and a dddD-type gene was found in Rhodococcus (32). Despite these studies, our knowledge of polar DMSP-catabolizing bacteria and their mechanisms for DMSP catabolism is still limited. Isolating new cultivable DMSP-catabolizing bacteria from polar oceans and investigating their DMSP catabolic pathways will enhance our understanding of DMSP catabolism in polar regions.
In this study, we screened DMSP-catabolizing bacteria from Arctic samples and found that strains from four genera (Psychrobacter, Pseudoalteromonas, Vibrio, and Alteromonas) could grow with DMSP as a sole carbon source. Moreover, the DMSP catabolic pathways of four representative strains were proposed on the basis of genomic and biochemical analyses, and the distribution of the key functional enzymes (DMSP CoA-transferase DddD and DMSP demethylase DmdA) involved in DMSP-catabolism in genera Psychrobacter, Pseudoalteromonas, and Vibrio was investigated using the Integrated Microbial Genomes & Microbiomes (IMG/M) system genome database.

RESULTS AND DISCUSSION

Isolation and identification of cultivable DMSP-utilizing bacteria from the Arctic samples.

Six samples were collected from the coastal area near the Kongsfjorden, including four surface seawater samples (samples 1–4) from different sites, a brown alga sample (sample 5), and a gammarid sample (sample 6) during the Chinese Arctic Yellow River Station Expedition in August 2017 (Fig. 1 and Table 1). Algae and gammarids are common in the coastal area of the Arctic, which were collected to detect whether the attached bacteria can catabolize DMSP. To isolate cultivable DMSP-utilizing bacteria from the Arctic samples, we screened strains using the agar medium with DMSP as the sole carbon source, and further cultured them in the liquid medium with DMSP as the sole carbon source to verify their DMSP-utilizing ability. In total, 79 bacterial strains that grew on DMSP as the sole carbon source were isolated. All these strains are Gammaproteobacteria and belong to four genera, Psychrobacter (47/79), Pseudoalteromonas (18/79), Vibrio (8/79), and Alteromonas (6/79) (Fig. 2 and Table 2).
FIG 1
FIG 1 Locations of the sampling sites in the Arctic. Blue circles indicate sites of sampling. Stations are plotted using Ocean Data View (Version ODV 5.3.0) (51).
FIG 2
FIG 2 The relative abundance of DMSP-utilizing bacteria isolated from the Arctic samples. Different colors indicate different genera.
TABLE 1
TABLE 1 Information of the sampling sites
SampleSiteLatitude (N)Longitude (E)Type of sample
1K278°58.00011°49.750Filter membrane
2K378°57.73611°54.237Filter membrane
3K678°52.33312°34.694Filter membrane
4K878°57.15712°09.815Filter membrane
5L78°55.1511°95.250Brown alga
6G78°55.1511°95.250Gammarid
TABLE 2
TABLE 2 The numbers of isolated strains from Arctic samples that could grow on DMSP as the sole carbon source
SampleGenusIsolate no.
1Pseudoalteromonas8
 Psychrobacter5
   
2Psychrobacter15
 Pseudoalteromonas4
   
3Psychrobacter10
 Alteromonas2
 Pseudoalteromonas5
   
4Alteromonas4
 Pseudoalteromonas1
   
5Psychrobacter13
 Vibrio1
   
6Vibrio7
 Psychrobacter4
Although all the strains belong to Gammaproteobacteria, bacteria isolated from different sites exhibited differences. Psychrobacter strains were present in all the samples except the seawater sample 4, Pseudoalteromonas and Alteromonas strains were isolated from only the seawater samples, and Vibrio strains were only from the brown alga and gammarid samples (Fig. 2 and Table 2). It has been reported that Gammaproteobacteria play an important role in absorbing soluble DMSP in the Arctic seawater (29), and bacteria in the genera Psychrobacter, Pseudoalteromonas, Vibrio, and Alteromonas were also found abundant in Svalbard Fjord previously (34, 35), suggesting that bacteria of these four genera play critical roles in DMSP catabolism in the Arctic. To the best of our knowledge, it has not been reported before that bacteria in genera Pseudoalteromonas and Alteromonas can grow with DMSP as the sole carbon source. In addition to polar regions, Gammaproteobacteria were also reported to be important participants in DMSP catabolism in the coastal region of Japan (36) and in Mariana Trench (37). However, our knowledge on the contribution of Gammaproteobacteria in global DMSP catabolism and the DMSP catabolic mechanisms of Gammaproteobacteria is still limited, especially for genera Psychrobacter, Pseudoalteromonas, Vibrio, and Alteromonas.
To further investigate the DMSP catabolic mechanisms of the isolated bacteria, four representative strains from different genera of Gammaproteobacteria, Pseudoalteromonas sp. K222D, Vibrio sp. G41H, Alteromonas sp. K632G, and Psychrobacter sp. K31L, which grew well on DMSP within their respective genus (Fig. 3), were selected and their genomes were sequenced.
FIG 3
FIG 3 The growth curves of the four representative strains cultured with DMSP as the sole carbon source. (A) Psychrobacter sp. K31L. (B) Pseudoalteromonas sp. K222D. (C) Alteromonas sp. K632G. (D) Vibrio sp. G41H. The growth curves of the strains cultured with DMSP (5 mM) as the sole carbon source are shown with solid squares. The growth curves of the strains cultured in the control medium without carbon source are shown with hollow triangles.

DMSP catabolic pathways in Psychrobacter sp. K31L.

Genomic analysis indicated that strain K31L contains a set of ddd genes (dddT, dddD, dddA, dddB and dddC), a set of dmd genes (dmdA, dmdB, dmdC and dmdD), and genes involved in acrylate catabolism (acuI, acuN, acuH and prpE) (Table 3). This suggests that this strain may adopt both the cleavage pathway and the demethylation pathway to catabolize DMSP, which is supported by the product detection. Both DMS (a product of the cleavage pathway, 127 ± 13 nmol DMS min−1 mg protein−1) and MT (a product of the demethylation pathway, 8 ± 3 nmol MT min−1 mg protein−1) were detectable when strain K31L was incubated with DMSP. Strain K31L released more DMS than the reported Psychrobacter sp. D2 (45 ± 2 nmol DMS min−1 mg protein−1), which utilizes DMSP-CoA ligase DddX to catabolize DMSP (14). Much more DMS was released by strain K31L than MT (Fig. 4), suggesting that the cleavage pathway may be dominant in this strain under the experimental conditions used. A similar phenomenon was reported in Ruegeria pomeroyi DSS-3 (38). In addition, we overexpressed the dddD gene in the cleavage pathway and the dmdA gene in the DMSP demethylation pathway of strain K31L in E. coli and purified the recombinant proteins (Fig. 5A). Both the recombinant DMSP CoA-transferase DddD and DMSP demethylase DmdA were active against DMSP (Fig. 5B and C), indicating that the dddD and the dmdA genes encode functional enzymes in strain K31L. The Km of DddD of strain K31L for DMSP was 12.8 mM, which is lower than that of DddD of strain Marinomonas sp. MWYL1 (Table 4) (13). The Km of DmdA of strain K31L for DMSP was 7.9 mM, which is similar to that of DmdA homologs of several Alphaproteobacteria (Table 4) (39, 40).
FIG 4
FIG 4 The production of DMS and MT in representative strains detected by GC. Bacteria were incubated in SCSM (500 μM DMSP) supplied with 0.45% glycerol (vol/vol) and 0.05% glucose (wt/vol) in a gas-tight sealing bottle at 20°C for 72 h, and then the produced DMS and MT were measured by GC. K31L, Psychrobacter sp. K31L; K222D, Pseudoalteromonas sp. K222D; K632G, Alteromonas sp. K632G; G41H, Vibrio sp. G41H. A two-sided Student's t test was used to assess statistically significant differences of the products of DMS and MT in strains (**, P < 0.01, *, P < 0.05).
FIG 5
FIG 5 Analyses of the in vitro activity of the key enzymes involved in DMSP catabolism from the representative strains. (A) SDS-PAGE analysis of the purified recombinant proteins of the key enzymes involved in DMSP catabolism from the representative strains. (B) Analysis of the enzymatic activity of the recombinant DddD proteins from Psychrobacter sp. K31L and Pseudoalteromonas sp. K222D by GC. The mixture without enzyme was used as the negative control. The DMS standard was used as the positive control. (C) Analysis of the enzymatic activity of the recombinant DmdA proteins from Psychrobacter sp. K31L and Vibrio sp. G41H by HPLC at 210 nm. The mixture without enzyme was used as the negative control. The MMPA standard was used as the positive control. K31L, Psychrobacter sp. K31L; K222D, Pseudoalteromonas sp. K222D, K632G, Alteromonas sp. K632G; G41H, Vibrio sp. G41H.
TABLE 3
TABLE 3 Predicted enzymes involved in DMSP catabolism in the four representative strains
StrainProtein IDDMSP degradation related enzymeCoverageIdentity
Vibrio sp. G41Horf04397AcuI (Nephila clavipes)99%52.61%
 orf02355AcuH (Roseovarius nubinhibens ISM)94%34.66%
 orf04056PrpE (Ruegeria pomeroyi DSS-3)98%57.10%
 orf04205DddA (Halomonas sp. HTNK1)93%37.82%
 orf01462DddB (Pseudomonas sp. J465)99%36.03%
 orf01096DddC (Psychrobacter sp. J466)96%29.46%
 orf01119DddP (Labrenzia sp. LZB033)89%22.76%
 orf02925DddT (Psychrobacter sp. J466)91%32.43%
 orf01914DmdA (Ruegeria pomeroyi DSS-3)85%24.77%
 orf00603DmdB (Marinobacter sp. HL-58)96%23.33%
 orf01826DddX (Psychrobacter sp. D2)88%24.29%
Psychrobacter sp. K31Lorf01851AcuI (Nephila clavipes)98%43.23%
 orf00482AcuN (Halomonas sp. HTNK1)80%40.36%
 orf01412AcuH (Roseovarius nubinhibens ISM)99%47.10%
 orf01366PrpE (Ruegeria pomeroyi DSS-3)98%41.87%
 orf00792DddA (Halomonas sp. HTNK1)93%36.76%
 orf00081DddB (Pseudomonas sp. J465)97%66.13%
 orf00080DddC (Psychrobacter sp. J466)100%92.94%
 orf00079DddD (Marinomonas sp. MWYL1)100%53.63%
 orf00078DddT (Psychrobacter sp. J466)100%88.55%
 orf01476DmdA (Ruegeria pomeroyi DSS-3)89%24.50%
 orf01622DmdB (Marinobacter sp. HL-58)98%50.37%
 orf00269DmdC (Halomonas beimenensis)99%40.47%
 orf01412DmdD (Pseudomonas fluorescens)94%28.05%
Alteromonas sp. K632Gorf03964AcuN (Halomonas sp. HTNK1)80%27.95%
 orf03968AcuH (Roseovarius nubinhibens ISM)98%33.84%
 orf02908PrpE (Ruegeria pomeroyi DSS-3)99%55.75%
 orf02363DddA (Halomonas sp. HTNK1)93%40.48%
 orf03423DddB (Pseudomonas sp. J465)96%37.33%
 orf01378DddC (Psychrobacter sp. J466)99%62.35%
 orf00954DddT (Psychrobacter sp. J466)94%33.97%
 orf03246DmdA (Ruegeria pomeroyi DSS-3)82%23.12%
 orf02455DmdB (Marinobacter sp. HL-58)97%21.65%
 orf01048DmdC (Halomonas beimenensis)100%40.83%
 orf03968DmdD (Ruegeria pomeroyi DSS-3)97%28.57%
Pseudoalteromonas sp. K222Dorf02895AcuI (Nephila clavipes)98%63.91%
 orf02696AcuH (Roseovarius nubinhibens ISM)96%39.84%
 orf01272PrpE (Ruegeria pomeroyi DSS-3)98%55.97%
 orf00404DddA (Halomonas sp. HTNK1)93%39.82%
 orf002638DddB (Pseudomonas sp. J465)100%74.55%
 orf002637DddC (Psychrobacter sp. J466)100%72.58%
 orf002641DddD (Marinomonas sp. MWYL1)99%71.02%
 orf002639DddT (Psychrobacter sp. J466)98%38.1%
 orf000727DmdA (Ruegeria pomeroyi DSS-3)83%24.45%
 orf01487DmdB (Marinobacter sp. HL-58)96%26.98%
 orf02696DmdD (Ruegeria pomeroyi DSS-3)97%29.8 %
 orf00867DddX (Psychrobacter sp. D2)90%23.14%
TABLE 4
TABLE 4 Kinetic parameters of DddD and DmdA homologs for DMSP
ProteinOrganismKm (mM)Kcat (s−1)Kcat/Km (M−1 s−1)Reference
DddDMarinomonas sp. MWYL1>40a12.6 ± 1.5NDb(13)
 Psychrobacter sp. K31L12.8 ± 0.23.0 ± 0.1234This study
 Pseudoalteromonas sp. K222D14.6 ± 0.38.2 ± 0.3562This study
DmdARuegeria pomeroyi DSS-35.4 ± 2.32.4450(39)
 Pelagibacter ubique HTCC106213.2 ± 2.08.1618(39)
 Ruegeria lacuscaerulensis ITI_11574.1 ± 0.4NDND(40)
 Psychrobacter sp. K31L7.9 ± 0.32.2 ± 0.02278This study
 Vibrio sp. G41H15.7 ± 1.61.1 ± 0.0370This study
a
Saturation was not observed at 40 mM.
b
No data available.
The dddD gene has been found in Alphaproteobacteria and Betaproteobacteria, and more frequently, in Gammaproteobacteria (4). This gene is usually located in a gene cluster that contains genes encoding the putative DMSP transporter DddT, the transcriptional regulator DddR, and some other enzymes involved in DMSP catabolism, including DddA, DddB, DddC, AcuN, and/or AcuH (4, 15). As shown in Fig. 6, the constitution and arrangement of ddd genes in the dddD gene cluster are different in different bacteria, such as those in Marinomonas sp. MWYL1 (15), Halomonas sp. HTNK1 (20), Pseudomonas J465, and Psychrobacter J466 (41). We found that the dddD gene in strain K31L is also located in a gene cluster. This cluster contains only four genes (dddT, dddD, dddB and dddC) and lacks the regulator gene dddR, which is similar to that of Psychrobacter sp. J446 (41).
FIG 6
FIG 6 Arrangement of ddd genes involved in DMSP catabolism in different bacterial strains. The dddD gene and other DMSP catabolism related genes from Marinomonas sp. MWYL1, Halomonas sp. HTNK1, Pseudomonas sp. J465, Psychrobacter sp. J466, Psychrobacter sp. K31L (this study, bold) and Pseudoalteromonas sp. K222D (this study, bold) are shown.
On the basis of the genomic analyses and experimental results, the DMSP catabolic pathways in strain K31L are proposed (Fig. 7A). When transported into the cell by the putative transporter DddT, DMSP is catabolized via two pathways. In the cleavage pathway, DMSP is first degraded by DddD into DMS and 3HP-CoA, and 3HP-CoA is further catabolized by DddA/DddB and DddC to acetyl-CoA (Fig. 7A). In the demethylation pathway, the DMSP demethylase, DmdA, first removes a methyl group from DMSP to form MMPA. MMPA is then further catabolized, via the intermediates MMPA-CoA and MTA-CoA, to acetaldehyde and MT by DmdB, DmdC, and DmdD/AcuH (Fig. 7A). Therefore, the strain K31L possesses two intact DMSP catabolic pathways.
FIG 7
FIG 7 Deduced pathways for DMSP catabolism in four representative strains. (A) Psychrobacter sp. K31L. (B) Pseudoalteromonas sp. K222D. (C) Alteromonas sp. K632G. (D) Vibrio sp. G41H. The DMSP catabolism-related genes found in the genomes are colored in red. The verified products MT and DMS are highlighted in blue. Proteins that presented enzymatic activity in vitro are highlighted in green. The unknown enzymes are indicated by a question mark (?).
Although a Psychrobacter strain, J446, isolated from Atlantic herring gut was shown to be able to produce DMS when growing on DMSP as the sole carbon source, and some ddd genes in this strain were revealed (41), an investigation of the DMSP catabolic pathways in Psychrobacter has not been reported. The above results indicate that the Psychrobacter strain K31L contains both the DMSP cleavage and demethylation pathways and catabolizes DMSP via both pathways.

DMSP catabolic pathways in Pseudoalteromonas sp. K222D.

Although one strain of Pseudoalteromonas has been found to have a dmdA gene in its genome (31), the DMSP catabolic pathways of Pseudoalteromonas have not been reported. Based on genomic analysis, the Pseudoalteromonas strain K222D contains a set of ddd genes (dddT, dddD, dddX, dddA, dddB, and dddC), three dmd genes (dmdA, dmdB, and dmdD), and three genes involved in acrylate catabolism (acuI, acuH, and prpE) (Table 3), indicating that this strain may contain both the cleavage pathway and the demethylation pathway to catabolize DMSP. This is supported by the experimental result that both products DMS (46 ± 0.4 nmol DMS min−1 mg protein−1) and MT (1 ± 0.2 nmol MT min−1 mg protein−1) were detectable when strain K222D was cultured with DMSP. This strain released much more DMS than MT under the experimental conditions (Fig. 4), suggesting that the cleavage pathway was likely dominant in K222D for DMSP catabolism under the tested experimental conditions. Moreover, the dddD gene, the dddX gene, and the dmdA gene of this strain were overexpressed in E. coli and the recombinant proteins were purified (Fig. 5A). The recombinant DMSP CoA-transferase DddD was active against DMSP (Fig. 5B) while DMSP-CoA ligase DddX was not, indicating that the dddD gene encodes a functional enzyme in strain K222D. The Km of the DddD of strain K222D for DMSP was 14.6 mM, which is similar to that of the DddD of strain K31L (Table 4) (13). The dddD gene in strain K222D also locates in a gene cluster. This cluster contains five genes (dddT, dddD, dddB, dddC, and dddR), which is similar to those of Marinomonas sp. MWYL1 (15) and Pseudomonas sp. J465 (41), but the arrangement of the genes is unique (Fig. 6). The activity of the recombinant DmdA protein from strain K222D against DMSP was not detectable. Because DddX and DmdA of strain K222D have very low sequence identities (less than 25%) to their functional homologs from other bacteria (Table 3), there may be a possibility that the dddX gene does not encode a true DddX enzyme and the dmdA gene does not encode a true DmdA enzyme in strain K222D. Alternatively, there may be another possibility that the inactivity of the recombinant DddX and DmdA resulted from the incorrect folding of the recombinant proteins.
According to the genomic analyses and experimental results above, the DMSP catabolic pathways in strain K222D are proposed (Fig. 7B). DMSP is first transported into the cell by the putative transporter DddT, and then catabolized through two pathways. In the cleavage pathway, DMSP is first degraded by DddD into DMS and 3HP-CoA, and 3HP-CoA is further catabolized by DddA/DddB into Mal-SA and then converted to acetyl-CoA by DddC (Fig. 7B). In the demethylation pathway, DMSP may be converted to MMPA-CoA by a demethylase and DmdB (Fig. 7B). However, no dmdC homolog is identified in its genome. Because MT is produced by strain K222D with added DMSP (Fig. 4) and this strain contains DmdD/AcuH homologs, strain K222D may recruit an enzyme with the same function as DmdC to catabolize MMPA-CoA, which needs further investigation.

DMSP catabolic pathways in Alteromonas sp. K632G.

Alteromonas strains have already been reported to be able to degrade DMSP (42); however, their DMSP catabolism pathways are unclear. On the basis of genomic and experimental analyses, we investigated the DMSP catabolism pathways of Alteromonas sp. K632G. Despite Alteromonas sp. K632G containing several dmd genes (dmdA, dmdB, and dmdD), ddd genes (dddT, dddA, dddB, and dddC), and genes involved in acrylate catabolism (acuN, acuH, and prpE), this strain does not contain any DMSP dethiomethylase gene in its genome (Table 3). However, DMS (4 ± 0.1 nmol DMS min−1 mg protein−1) was detectable when strain K632G was incubated with DMSP, suggesting that this strain likely adopts a novel DMSP dethiomethylase to cleave DMSP to generate DMS. In addition, a similar amount of MT (4 ± 0.1 nmol MT min−1 mg protein−1, Fig. 4) was also produced when strain K632G was incubated with DMSP, suggesting that this strain also catabolized DMSP via the demethylation pathway. When the dmdA gene of this strain was overexpressed in E. coli (Fig. 5A), the activity of the recombinant DmdA was not detectable, maybe because of the incorrect folding of the recombinant protein or the existence of a novel DMSP demethylase considering the low sequence identity (less than 25%, Table 3) of DmdA of strain K632G to its functional homologs from other bacteria.
On the basis of these data, the DMSP catabolic pathways in strain K632G are proposed (Fig. 7C). DMSP is transported into the cell by the putative transporter DddT and catabolized by two pathways. In the cleavage pathway, DMSP may be first degraded into DMS and acrylate by a novel DMSP dethiomethylase possessing insignificant sequence similarity with known DMSP dethiomethylases. Acrylate is further metabolized by AcuN/PrpE to acryloyl-CoA, then converted to 3HP-CoA. 3HP-CoA is catabolized by DddA/DddB into Mal-SA and then converted to acetyl-CoA by DddC (Fig. 7C). In the demethylation pathway, DMSP may be sequentially catabolized by a demethylase, DmdB, DmdC and DmdD/AcuH to MMPA, MMPA-CoA, MTA-CoA, and the final products acetaldehyde and MT.
Previous studies have shown that enzymes involved in DMSP cleavage are diverse, and seven DMSP dethiomethylases have so far been reported (4, 14, 17). Our analysis suggests that it is likely that strain K632G contains a novel DMSP dethiomethylase, which warrants further investigation.

DMSP catabolic pathways in Vibrio sp. G41H.

Despite that Vibrio species have been reported to catabolize DMSP (14, 42, 43), the DMSP catabolic pathways in Vibrio have not been reported. Here, we investigated the DMSP catabolic pathways in Vibrio sp. G41H. According to genomic analysis, Vibrio sp. G41H contains a set of ddd genes involved in DMSP cleavage pathway (dddT, dddP, dddX, dddA, dddB, and dddC), a set of genes involved in acrylate catabolism (acuI, acuH, and prpE), and three genes involved in the DMSP demethylation pathway (dmdA, dmdB, and AcuH) (Table 3). Thus, this strain contains genes involved in both the cleavage pathway and the demethylation pathway, and may catabolize DMSP via both pathways, which is supported by the result that both DMS (5 ± 0.8 nmol DMS min−1 mg protein−1) and MT (5 ± 0.6 nmol MT min−1 mg protein−1) were detectable when strain G41H was incubated with DMSP. Compared to Psychrobacter sp. K31L and Pseudoalteromonas sp. K222D, strain G41H possessed relatively weaker DMSP catabolic capacity (Fig. 4), which may explain its weak growth on DMSP (Fig. 3D). The dddP gene, the dddX gene, and the dmdA gene were then overexpressed in E. coli and the recombinant proteins were purified (Fig. 5A). While DmdA exhibited in vitro activity against DMSP (Fig. 5C), the activity of DMSP dethiomethylase DddP or DMSP-CoA ligase DddX against DMSP was not detectable, suggesting the incorrect folding of the recombinant protein or the possible existence of a novel DMSP dethiomethylase.
On the basis of these data, the DMSP catabolic pathways in strain G41H are proposed (Fig. 7D). When the putative transporter DddT transports DMSP into the cell, DMSP might be catabolized by two pathways. In the cleavage pathway, DMSP might first be degraded by a DMSP dethiomethylase into DMS and acrylate. Acrylate could be converted to acryloyl-CoA by PrpE, and acryloyl-CoA could be converted to propionyl-CoA by AcuI or to 3HP-CoA by AcuH. The 3HP-CoA is catabolized into Mal-SA by DddA/DddB and then to acetyl-CoA by DddC (Fig. 7D). In the demethylation pathway, DMSP is converted to MMPA-CoA by DmdA and DmdB (Fig. 7D). However, no dmdC homolog is identified in its genome. Because MT is produced by strain G41H with added DMSP (Fig. 4) and this strain contains AcuH homolog, this strain may recruit an enzyme with the same function as DmdC to catabolize MMPA-CoA, which needs further confirmation.

Distribution of key enzymes involved in DMSP catabolism in the representative genera.

With the sequences of the functional enzymes (DMSP CoA-transferase DddD homologs of Psychrobacter sp. K31L and Pseudoalteromonas sp. K222D and DMSP demethylase DmdA homologs of Psychrobacter sp. K31L and Vibrio sp. G41H) as queries, the distributions of DddD in genera Psychrobacter and Pseudoalteromonas and DmdA in genera Psychrobacter and Vibrio were investigated using the IMG/M system genome database. All the genomes of Psychrobacter (63), Pseudoalteromonas (197), and Vibrio (1313) were downloaded and used for analysis. For the DMSP CoA-transferases involved in the DMSP cleavage pathway, homologs of DddD of Psychrobacter sp. K31L were found in only 3 of the 63 genomes of genus Psychrobacter, and no homologs of DddD of Pseudoalteromonas sp. K222D was found in the 197 genomes of the genus Pseudoalteromonas (Fig. 8). In contrast, homologs of DmdA of Psychrobacter sp. K31L (61/63) and Vibrio sp. G41H (1264/1313) are widely distributed in the genomes within their respective genus (Fig. 8). These results suggest that a high proportion of strains of Psychrobacter and Vibrio likely contain the DMSP demethylation pathway, while only a small portion of Psychrobacter has the potential to catabolize DMSP with the cleavage pathway.
FIG 8
FIG 8 Relative abundance of key enzymes involved in DMSP catabolism within their respective genus. K31L, Psychrobacter sp. K31L; K222D, Pseudoalteromonas sp. K222D; G41H, Vibrio sp. G41H.
MRC and SAR11 clade of Alphaproteobacteria are considered the major DMSP-catabolizing groups in the marine environment, and current knowledge on DMSP catabolic pathways is mainly from studies on Alphaproteobacteria (4, 22, 44). Despite several studies suggested that Gammaproteobacteria also make great contributions to DMSP catabolism in various environments such as the Arctic, salt marsh, and estuary (29, 42, 45), the DMSP catabolic pathways of Gammaproteobacteria are rarely studied. It has been reported that strains of Psychrobacter, Vibrio and Alteromonas could degrade DMSP into DMS (4143), but their ability to catabolize DMSP through the demethylation pathway has not been evaluated. Our genomic analyses indicate that a high proportion (>90%) of bacteria of genera Psychrobacter and Vibrio contain DmdA homologs, suggesting that bacteria of the two genera may be important DMSP-catabolizing groups in global oceans.

Conclusion.

DMSP plays an important role in the global sulfur cycle. Although there is a great number of bacterial strains that are reported to catabolize DMSP, only a few cultivable DMSP-utilizing strains isolated from polar regions are reported (31, 32). In this study, we collected samples from the Arctic during summer, and found that strains in the genera Psychrobacter, Pseudoalteromonas, Alteromonas, and Vibrio could grow with DMSP as the sole carbon source. Moreover, the DMSP catabolic pathways in four representative strains from these four genera were proposed. Bioinformatic analysis indicated that a high proportion of bacteria of genera Psychrobacter and Vibrio may be able to catabolize DMSP. Our results also suggest that novel enzymes involved in DMSP catabolism may exist in Pseudoalteromonas, Alteromonas, and Vibrio, which warrants further investigation.

MATERIALS AND METHODS

Sample collection.

Kongsfjorden is a glacial fjord located on the west coast of Spitsbergen in the Svalbard archipelago. Six samples were collected from the coastal area near the Kongsfjorden (Fig. 1). Detailed information of the samples was shown in Table 1. Surface seawater samples were filtered through polycarbonate membranes with 0.22-μm pores (Millipore Co., USA). Filtered membranes were stored in sterile tubes (Corning Inc., USA) at 4°C. The brown alga sample and gammarid sample were collected using a grab sampler and stored in airtight sterile plastic bags at 4°C.

Isolation and identification of DMSP-utilizing bacteria.

The dilution-plating method was used to isolate DMSP-utilizing bacteria from the samples. Filtered membranes of surface seawater or two grams (wet weight) of brown alga or gammarid sample were incubated in 20 ml sterilized artificial seawater (ASW) at 10°C with shaking at 180 rpm for 4–5 h. The ASW contained 3% (wt/vol) sea salts (Sigma, USA). The suspension was further serially diluted 10-fold (up to the 10−4 dilution) using sterile ASW. Aliquots of 200 μl diluted sample (100-10−4 dilution) were then spread onto the agar plates containing the sole carbon source medium (SCSM, pH 8.0) that comprised (mg/liter) ammonium chloride (500), sodium chloride (30,000), manganous chloride hexahydrate (3,000), potassium sulfate (2,000), dipotassium hydrogen phosphate (200), calcium chloride (10), ferric chloride hexahydrate (6), sodium molybdate (5), cupric chloride dihydrate (4), Tris base (6,000) and was supplemented with vitamin solution (1 ml/liter) and DMSP hydrochloride (TCI, Japan) to 5 mM as the sole source of carbon and energy. The plates were then incubated at 10°C for 20–30 days. Colonies showing different morphologies on the plates were selected and further purified by streaking on agar plates containing the same SCSM for several passages. The purified isolates were further cultured in liquid SCSM at 20°C with shaking to test their DMSP-utilizing ability.
The 16S rRNA genes of the representative strains were extracted from the draft genome sequences and those of the other strains were amplified using the 27F and 1492R primers (46). Calculation of pairwise similarity values for the sequences of the 16S rRNA genes was performed on the Ezbiocloud server (http://www.ezbiocloud.net/identify).

Measurement of DMS and MT.

Bacteria were incubated in SCSM (DMSP as the carbon source with a final concertation of 500 μM) supplied with glycerol (61.6 mM) and d-glucose (2.8 mM) in a gas-tight sealing bottle at 20°C for 72 h, and then the produced DMS and MT were measured. The mixture without DMSP and the mixture without bacteria were set as controls. The DMS standard (Sigma, America) and MT standard (Sigma, America) were used as positive controls. DMS and MT were measured using gas chromatograph (GC-2030, Shimadzu, Japan) according to the method described by Zhang et al. (47). In brief, the sample was collected into a glass bubbling chamber through a GF/F filter. Sulfur gases were sparged from the culture solution with a stream of nitrogen and trapped into filling TenaxTA trap tube under −10°C. The trapped gases were desorbed over 110°C and analyzed on GC equipped with a flame photometric detector. A 3 m × 3 mm glass column packed with 10% DEGS on Chromosorb W-AW-DMCS was used to separate sulfur gases at 70°C. A seven-point calibration curve of DMS or MT standards was used (3). The detection limit for DMS and MT were 0.5 nmol and 50 nmol, respectively. The cells were lysed by ultrasonication and protein content in the cell extract was determined by Pierce BCA Protein assay kit (Thermo, USA). DMS and MT productions were expressed as nmol min−1 mg protein−1. Statistical analysis was carried out using Excel. A two-sided Student's t test was used to analyze whether the products of DMS and MT were statistically significantly different.

Genome sequencing and gene annotation.

The genomes of four representative strains were sequenced through an Illumina Hiseq platform. Genome assembly was performed with ABySS v2.0.2 with multiple-Kmer parameters (48). Gene annotation was carried out using the National Center for Biotechnology Information Search database (NCBI) Prokaryotic Genome Annotation Pipeline (PGAP). The completeness of the draft genomes was calculated by the CheckM (49). The completeness of the draft genomes of Psychrobacter sp. K31L, Pseudoalteromonas sp. K222D, Alteromonas sp. K632G, and Vibrio sp. G41H was 99.95%, 100.00%, 99.59% and 100.00%, respectively. BLASTp program was used to identify the putative enzymes in the representative strains with the thresholds of coverage ≥ 80%, similarity ≥ 20% and E value ≤ 1e−10.

Gene cloning and protein expression and purification.

Genes predicted as DMSP CoA-transferase, DMSP-CoA ligase, DMSP dethiomethylase, or DMSP demethylase were cloned from the genomes of the four representative strains via PCR and overexpressed in E. coli BL21(DE3) cells using the pET-22b vector that contains a C-terminal His-tag for protein purification. The E. coli cells were cultured in the lysogeny broth (LB) medium with 0.1 mg/ml ampicillin at 37°C to an OD600 of 0.8–1.0 and then induced at 15°C for 14 h with 0.2 mM isopropyl-β-d-thiogalactopyranoside (IPTG) as the inducer. Recombinant proteins were purified with Ni2+-NTA resin (Qiagen, Germany), followed by desalination on PD-10 Desalting Columns (GE Healthcare, USA).

Enzyme assays.

The activity of DMSP CoA-transferase, DMSP-CoA ligase or DMSP dethiomethylase was determined by measuring DMS production using GC. The enzymatic activity of DddP was assayed according to the method described by Todd et al. (50). In brief, the purified DddP enzyme (1 mg/ml) was incubated with 5 mM DMSP and 100 mM Tris-HCl (pH 8.0). The reaction was performed at 30°C for 12 h. The activity of DddD was measured according to the method described by Acolombri et al. (13). In brief, the DddD (1 mg/ml) and cofactor acetyl-CoA (1 mM) were added in the reaction mixture of 5 mM DMSP and 100 mM Tris-HCl (pH 8.0). The reaction was performed at 30°C for 0.5 h. The activity of DmdA was assayed according to the method described by Reisch et al. (39). In brief, the recombinant DmdA enzyme (1 mg/ml) and 5 mM DMSP, 1 mM ethylenediamine tetraacetic acid, 2 mM dithiothreitol, 0.685 mM tetrahydrofolate, and 400 mM HEPES (pH 7.5) were incubated at 37°C for 1 h, and then the product MMPA was measured by high performance liquid chromatography (HPLC, Shimadzu, Japan) on a SunFire C18 column (Waters, USA) with a linear gradient of 2–20% acetonitrile in 50 mM ammonium acetate (pH 5.5) over 24 min at 210 nm.

Bioinformatics.

The IMG/M system genome database was used to search for the distribution of key enzymes involved in DMSP catabolism in genome-sequenced bacterial isolates. The key enzymes involved in DMSP catabolism in the representative strains were used as the query sequences with an E value cutoff 1e−50, a coverage cutoff 80% and a similarity cutoff 20%.

Data availability.

The draft genome sequences of Psychrobacter sp. K31L, Pseudoalteromonas sp. K222D, Alteromonas sp. K632G, and Vibrio sp. G41H were deposited in the NCBI genome database under the project accession numbers JAGKSC000000000, JAGGDL000000000, JAGGDM000000000 and JAGGDK000000000, respectively.

ACKNOWLEDGMENTS

We thank Caiyun Sun from State Key Laboratory of Microbial Technology of Shandong University for help and guidance in HPLC. This work was supported by the National Science Foundation of China (42076229, 31630012, U1706207, 91851205, 31800107), the National Key R&D Program of China (2018YFC1406700), and the Program of Shandong for Taishan Scholars (tspd20181203).

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Information & Contributors

Information

Published In

cover image Applied and Environmental Microbiology
Applied and Environmental Microbiology
Volume 88Number 225 January 2022
eLocator: e01806-21
Editor: Maia Kivisaar, University of Tartu
PubMed: 34788071

History

Received: 13 September 2021
Accepted: 12 November 2021
Accepted manuscript posted online: 17 November 2021
Published online: 25 January 2022

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Keywords

  1. the Arctic
  2. DMSP
  3. marine bacteria
  4. catabolic pathways
  5. Gammaproteobacteria

Contributors

Authors

Shan Zhang
State Key Laboratory of Microbial Technology, Shandong University, Qingdao, China
College of Marine Life Sciences, and Frontiers Science Center for Deep Ocean Multispheres and Earth System, Ocean University of China, Qingdao, China
Laboratory for Marine Biology and Biotechnology, Qingdao National Laboratory for Marine Science and Technology, Qingdao, China
Hai-Yan Cao
State Key Laboratory of Microbial Technology, Shandong University, Qingdao, China
Nan Zhang
School of Bioengineering, Qilu University of Technology (Shandong Academy of Sciences), Jinan, China
Zhao-Jie Teng
State Key Laboratory of Microbial Technology, Shandong University, Qingdao, China
Yang Yu
State Key Laboratory of Microbial Technology, Shandong University, Qingdao, China
Zhi-Bin Wang
State Key Laboratory of Microbial Technology, Shandong University, Qingdao, China
Peng Wang
College of Marine Life Sciences, and Frontiers Science Center for Deep Ocean Multispheres and Earth System, Ocean University of China, Qingdao, China
Laboratory for Marine Biology and Biotechnology, Qingdao National Laboratory for Marine Science and Technology, Qingdao, China
Hui-Hui Fu
College of Marine Life Sciences, and Frontiers Science Center for Deep Ocean Multispheres and Earth System, Ocean University of China, Qingdao, China
State Key Laboratory of Microbial Technology, Shandong University, Qingdao, China
Laboratory for Marine Biology and Biotechnology, Qingdao National Laboratory for Marine Science and Technology, Qingdao, China
State Key Laboratory of Microbial Technology, Shandong University, Qingdao, China
College of Marine Life Sciences, and Frontiers Science Center for Deep Ocean Multispheres and Earth System, Ocean University of China, Qingdao, China
Laboratory for Marine Biology and Biotechnology, Qingdao National Laboratory for Marine Science and Technology, Qingdao, China
College of Marine Life Sciences, and Frontiers Science Center for Deep Ocean Multispheres and Earth System, Ocean University of China, Qingdao, China
Laboratory for Marine Biology and Biotechnology, Qingdao National Laboratory for Marine Science and Technology, Qingdao, China

Editor

Maia Kivisaar
Editor
University of Tartu

Notes

The authors declare no conflict of interest.

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