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Degradation potential and diversity of oil-degrading bacteria isolated from the sediments of the Jiaozhou Bay, China
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Wei Gao1, 2, †, Xiangxing Gao2, 3, †, Tiezhu Mi4, 5, 6, Bin Han2, Yiran Zhang2, Xinzi Li2, Xiaofei Yin2, Chengjun Sun2, Qian Li2, Zhisong Cui2, Xiao Luan2, Zhigang Yu5, 6, Li Zheng2, 6, *
Acta Oceanologica Sinica | 2019, 38(6) : 54 - 64
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Acta Oceanologica Sinica | 2019, 38(6): 54-64
• Marine Biology •
Degradation potential and diversity of oil-degrading bacteria isolated from the sediments of the Jiaozhou Bay, China
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Wei Gao1, 2, †, Xiangxing Gao2, 3, †, Tiezhu Mi4, 5, 6, Bin Han2, Yiran Zhang2, Xinzi Li2, Xiaofei Yin2, Chengjun Sun2, Qian Li2, Zhisong Cui2, Xiao Luan2, Zhigang Yu5, 6, Li Zheng2, 6, *
Affiliations
  • 1 College of Marine Life Sciences, Ocean University of China, Qingdao 266003, China
  • 2 Marine Ecology Research Center, First Institute of Oceanography, Ministry of Natural Resources, Qingdao 266061, China
  • 3 National Deep Sea Center, Qingdao 266237, China
  • 4 College of Environmental Science and Engineering, Ocean University of China, Qingdao 266100, China
  • 5 Key Laboratory of Marine Chemical Theory and Technology, Ministry of Education, Qingdao 266100, China
  • 6 Laboratory for Marine Ecology and Environmental Science, Pilot National Laboratory for Marine Science and Technology (Qingdao), Qingdao 266237, China
Published: 2019-06-25 doi: 10.1007/s13131-019-1353-2
Outline
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A great deal of oil contaminated the shoreline by the Qingdao oil pipeline explosion in 2013. The four oil-degrading consortia were enriched from sediment samples with crude oil as sole carbon and energy sources. The biodiversity and community analysis showed that the Luteibacter, Parvibaculum and a genus belonging to Alcanivoracaceae were found predominant bacteria in the four consortia, which belonged to Proteobacteria. Nine strains exhibiting distinct 16S rRNA gene sequences were isolated from the consortia. These strains were identified to eight genera based on 16S rRNA gene sequences. Five of the nine strains degraded more than 30% of the crude oil in two weeks by gravimetric method. From the analysis of GC-MS, most of the isolated strains tended to degrade n-alkanes rather than PAHs. Five strains showed high degrading ability of the total n-alkanes. Only Strain D2 showed great PAHs degrading ability and the degrading rates ranged from 34.9% to 77.5%. The sequencing analysis of the oil-degrading consortia confirmed that the genus of Alcanivorax was one of the dominant bacteria in Consortia A and E and Strain E4 might be one of the dominant bacteria. The strains obtained in this study demonstrated the potential for oil bioremediation in oil-contaminated beach ecosystems.

oil spill  /  biodegradation  /  microbial consortium  /  dominant bacteria
Wei Gao, Xiangxing Gao, Tiezhu Mi, Bin Han, Yiran Zhang, Xinzi Li, Xiaofei Yin, Chengjun Sun, Qian Li, Zhisong Cui, Xiao Luan, Zhigang Yu, Li Zheng. Degradation potential and diversity of oil-degrading bacteria isolated from the sediments of the Jiaozhou Bay, China[J]. Acta Oceanologica Sinica, 2019 , 38 (6) : 54 -64 . DOI: 10.1007/s13131-019-1353-2
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1 Introduction
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Millions of liters of petroleum hydrocarbons from both natural and anthropogenic sources contaminated the marine environment annually (Hassanshahian et al., 2012). Bioremediation technologies to degrade these pollutants had long been investigated in laboratory and in field studies (Mortazavi et al., 2013; Cai et al., 2013). However, new knowledge on the microbial physiological activities was required to improve the degradation efficiency in practice (Samanta et al., 2002). The key step to enhance the efficiency was to eliminate the adverse effects of the biotic and abiotic factors on the functional communities. It was generally acknowledged that the abundant bacteria were the best adapting to the environment. So screening the predominant microorganisms with high degrading rate should be a sound approach. To screen the dominant bacteria, the abundance of each bacterium should be exhibited firstly and high-throughput sequencing analysis provided an efficient way to get the abundance information. Combining the sequencing analysis and isolation of bacteria would give a sight to understand the abundance of each isolate. The dominant bacteria would be more efficiently screened based on the abundance information.
Changes in composition and abundance of oil lead the rapid succession on the associated bacterial community (Mason et al., 2014). The bacteria would be totally different between the fresh and weathered oil. Most of the studies used oil samples collected after more than 10 d after oil-spill, and in this circumstance the oil composition varies significantly due to weathering effect (Fingas, 2012; Kleindienst et al., 2015). The consortia in these samples would change to adapt to the altered conditions. The dominant strains were more suitable for the biodegradation of weathered oil, but not for the quick response of oil-spill. This may be one reason for the low efficiency of bioremediation in large scaled application. The Qingdao blowout on November 22, 2013 (known as “11.22”) resulted in an intermittent spill of an estimated 2 000 metric tons of crude oil on the seashore. Our team collected the sediment samples polluted with fresh oil. We wanted to study whether there were differences in oil-degrading bacteria isolation between these samples and the weathered oil polluted samples. And then we expected to isolate the dominant strains with the high oil-degrading ability under the direction of high through sequencing analysis. All the strains we screened would be useful for directing the cleanup in oil-contaminated beach ecosystems.
2 Materials and methods
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2.1 Sites and sampling protocol
After the “11.22” explosion in Qingdao on November 22, 2013, the neighboring seashore was contaminated by heavy crude oil. Within the following week, we collected sediments from four sites (Sites A, B, C, D and E) along the oil-polluted seashore (Fig. A1). The consortium from Site A (Site C, Site D and Site E) which showed high degrading performance was defined as Consortium A (C, D and E), specifically shown in Table A1. Samples were collected using sterilized, site-specific sampling shovels. Excavated samples were wrapped in aluminum foil, immediately transported to the lab on ice and kept at 4°C before further processing. Each site consisted of sandy sediment with an oil content of 0.92–1.40 g per 100 g of sediment (Table A1).
2.2 Isolation of the oil-degrading bacteria
A total of 2 g contaminated sediment was added to 100 mL ONR7a medium with 1% (w/v) crude oil as the sole carbon and energy source (Dyksterhouse et al., 1995). The medium was autoclaved in 121°C for 15 min. After incubation for two weeks under aerobic conditions at 25°C, cultures that showed visible degrading changes to the oil were transferred as a 2% inoculum to fresh medium as above, and cultivated under the same conditions. This consortium enrichment was repeated three times to obtain a stable bacterial consortium. A culture without added sediment was used as a negative control. The consortia that caused most visible degradation of the oil from Sites A, C, D and E were defined as Consortia A, C, D and E respectively.
Then the culture (100 μL) was serially diluted and plated on M8 agar plates (Cui et al., 2008) and incubated at 25°C for 5 d. Bacterial strains displaying different morphologies were streaked on fresh M8 plates for purification. The consortia and all isolates were stored in 20% of glycerol in cryogenic vial at –80°C.
2.3 DNA extraction and Illumina MiSeq sequencing
DNA was extracted from cell biomass pelleted from 10 mL of the final cultures through centrifugation at 9 660 g for 10 min. Total genomic DNA was extracted following the method described by Rochelle (Rochelle, 2001). The V3–V4 region of the 16S ribosomal RNA gene was amplified by PCR (95°C for 2 min, followed by 25 cycles at 95°C for 30 s, 55°C for 30 s, and 72°C for 30 s and a final extension stage at 72°C for 10 min) using primers 338F and 806R. All PCR reactions were performed in triplicate with a reaction volume of 20 μL (4 μL of 5× FastPfu buffer, 2 μL of 2.5 mmol/L dNTPs, 0.8 μL of each primer (5 μmol/L), 0.4 μL of FastPfu Polymerase, and 10 ng of template) on an ABI GeneAmp® 9700 thermal cycler. Products were run on 2% agarose gels, from which amplicons were extracted, purified using the AxyPrep DNA Gel Extraction Kit (Axygen Biosciences, Union City, CA, US) according to the manufacturer’s instructions, and quantified using QuantiFluorTM-ST (Promega, US). Purified amplicons were pooled in equimolar mixtures and paired-end sequenced (2×250 bp) on an Illumina MiSeq platform according to standard protocols.
2.4 Bacterial community analysis
Raw fastq files were demultiplexed, quality-filtered using QIIME (version 1.17) with the following criteria: (1) The 300 bp reads were truncated at any site with an average quality score <20 over a 50 bp sliding window, discarding any reads with less than 50 bp remaining; (2) exact barcode matching, two nucleotide mismatch in primer matching, reads containing ambiguous characters were removed; (3) only sequences that overlapped by more than 10 bp were assembled according to their overlap sequence, and reads that could not be assembled were discarded.
Operational taxonomic units (OTUs) were clustered with a 97% similarity cutoff using UPARSE (Version 7.1 http://drive5.com/uparse/), chimeric sequences were identified and removed using UCHIME. Each 16S rRNA gene sequence was taxonomically classified against the SILVA (SSU115) 16S rRNA database using the RDP Classifier (http://rdp.cme.msu.edu/) with a confidence threshold of 70% (Amato et al., 2013). All the sequences data were submitted to the Genebank and the Bioproject accession numbers were PRJNA399603. The alpha-diversity indices (ACE, Chao1, Shannon and Simpson) were analyzed with Mothurv (version 1.30.1) at a 97% similarity level (Schloss et al., 2011).
2.5 Identification and phylogenetic analysis
Purified strains were cultured in M8 medium at 25°C for 3 d (cell concentration at OD600: 1.0–1.2). Genomic DNA was extracted and 16S rRNA amplified as above from pellets obtained by centrifugation at 9 660 g for 5 min, except for the primer set replaced by 16SR and 16SF (Cui et al., 2008). The amplified 16S rRNA gene fragments were sequenced using the ABI 3730xl sequencing system by TsingKe Biological Technology (Qingdao). Sequences were aligned using BLAST and used to construct the phylogenetic tree according to the methods described by Shao et al. (2010). The dominant Strain E4 isolated was deposited in China General Microbiological Culture Collection Center with the number CGMCC 1.16160.
2.6 The characterization of Thioclava isolates
The six strains belonged to genus Thioclava were discriminated by the house keep gene and multilocus sequence analysis. PCR amplification of gyrB, rpoD, recA, trpB, and dnaK gene were performed using the primers as described previously (Lai et al., 2014; Liu et al., 2017). The PCR products were sequenced with the ABI 3730xl sequencing system by TsingKe Biological Technology (Qingdao). All sequences were submitted to GenBank database. The accession numbers were assigned and listed in Table A2. The type strain Rhodovulum sulfidophilum DSM 1374T was chosen as an outgroup for the phylogenetic analysis. The multilocus sequence analysis (MLSA) was followed the study of Liu et al. (2017). Phylogenetic tree was constructed by neighbor-joining method based on MLSA sequences with MEGA software (Version 7.0.26). Bootstrapping analysis was carried out with 1 000 replicated. And the similarities of different genes were calculated by the DNAMAN software (Version 6.0.3).
2.7 Degradation rate and analysis of characteristics
Next, the rates at which the bacterial consortia and isolated strains degraded crude oil were quantified. All four consortia and 9 of the 15 isolated strains with distinct 16S rRNA gene sequence were tested. Of each enriched consortium or isolate, 1 mL was transferred to 100 mL of sterilized ONR7a medium containing 1% (w/v) crude oil (1% inoculum volume) in three replicates, and incubated at 25°C on a rotator shaker for two weeks. After this period of biodegradation, the total residual hydrocarbons and their derivatives were extracted from the control (medium without any inoculum) and the degraded medium using 50 mL of dichloromethane.
The rate at which oil was degraded was calculated using the residual weight of oil, determined by gravimetric analysis as described by Zheng et al. (2012). Degrading rates (A) were obtained using the formula:
$A = \left[ {\left({{{{m}}_0} - {{{m}}_1}} \right) \div {{{m}}_0}} \right] \times 100\%, $
where m0 is the residual weight of the control and m1 is the residual weight of the sample after degradation.
More specifically, the total utilization of alkanes and polycyclic aromatic hydrocarbons (PAHs) were quantified using the gas chromatography–mass spectrometer (GC-MS) method. One milliliter of the residual organic phase was dehydrated in a column with 2 g of anhydrous Na2SO4 and filtered with a 0.22 μm nylon membrane (JINTENG, Tianjin, China). After evaporation under a stream of nitrogen, the residue was re-dissolved in chromatography-grade n-hexane. N-Tetracosane-D50 and P-Terphenyl-D14 were set as internal standards (10 μg/mL each). The samples were then analyzed using a 6890A gas chromatograph (Agilent Technologies) in an HP-5 MS capillary column (30 m long×250 μm internal diameter, 0.22 μm thickness) and a 5 973 mass spectrometer equipped with a quadrupole axis detector. Hydrocarbons were quantified following the protocols described by Zheng et al. (2012) and degradation rates calculated as a percentage relative to each hydrocarbon’s concentration in the control.
The utilization of alkanes and PAHs as a sole carbon and energy source was determined. One of the following compounds was contained in the culture. The compounds were Hexadecane, Dotriacontane, Napthalene, Dibenzothiopene, Fluorene, Phenanthrene, and Pyrene. The bacteria were centrifugated, washed and resuspended in ONR7a medium. The culture, containing 0.3% (w/v) alkane and PAH respectively, was inoculated by 2% (v/v) bacterial suspension and incubated on a rotary shaker at 25°C for 7 d. The medium without innoculation was served as control. All the experiments were performed in triplicate. The growth was obtained by measurement of the optical density at 600 nm. The utilization of carbon sources was measured by the increase of the bacteria (Balachandran et al., 2012).
3 Results
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3.1 Structure of oil-degrading microbial consortia
Bacterial consortia that visibly degraded oil yielded a total of 55 548 effective reads with a length of 427–440 bp (Table 1). Sequence coverage was 99.9%, indicating that the sequencing depth captured the composition of the prokaryotic consortia well. The RDP classifier gave a total of 262 OTUs, with Consortium A containing 86 OTUs and Consortia C, D, and E less than 70 OTUs each (Table 1). Moreover, community richness was considerably higher in Consortium A than in the other consortia, while biodiversity was highest in Consortium D (Table 1). Consortia A, C and E showed similar levels of biodiversity (Simpson index 0.23–0.28, Table 1).
The bacterial community composition was analyzed at different taxonomic levels (Figs 1 and 2). Across all the consortia, eight phyla were identified, with Proteobacteria the most abundant phylum in all the samples (98% in Consortium A, 90% in Consortium C, 98% in Consortium D and 95% in Consortium E; Fig. 1). Consortia C and E showed a broadly different structure to Consortia A and D. Bacteroidetes was the second most abundant phylum, at a similar abundance in both Consortia C (4.3%) and E (4.7%), while Actinobacteria represented 5.4% of Consortium C but only 0.6% in Consortium E (Fig. 1).
At a lower taxonomic level, 80 genera were identified (Fig. 2). The different sites again showed substantial differences in community structure. A genus belonging to Alcanivoracaceae (Alcanivoracaceae-norank in Fig. 2) was the main genus in Consortia A and E, reaching up to 45.1% and 40.7%. The other dominant taxa (>10%) were totally different in the four consortia (Fig. 2). In Consortium A, Thalassospira accounted for 23.3% of the reads, while in Consortium E, Defluviimonas (17.2%), other genus belonging to Rhodobacteraceae (14.2%), and Parvibaculum (11.5%) were the most abundant genera after Alcanivoracaceae-norank. In contrast, in Consortium C the dominant genus was Luteibacter (51%), which contributed <1.1% to other consortia. Consortium D showed a richer structure, with 71.5% of reads consisting of three main genera (Parvibaculum 34%, genus belonging to Erythrobacteraceae 18.9%, genus belonging to Rhodobacteraceae 18.6%; Fig. 2).
3.2 Identification of oil-degrading bacteria
A total of 15 strains (8 genera in Proteobacteria) were isolated and identified (Table 2, Fig. 3). All the strains belonged to the phylum of Proteobacteria and Alphaproteobacteria accounted for 80% of the 15 strains. One strain, C3, may be a novel strain due to its relatively low similarity (98.37%) with the type strain (Thioclava pacifica DSM 10166T) (Stackebrandt and Ebers, 2006). All the 16S rRNA gene sequences of the 15 strains were submitted to the National Center for Biotechnology Information (GenBank accession numbers in Table 2).
The strains belonging to genus Thioclava showed high similarity in 16S rRNA gene sequence. In order to discriminate the six strains, five house-keeping genes were used for the phylogenetic analysis. In comparison with 16S rRNA gene tree, the phylogenetic trees of Strains C3, C4, and C5 showed deep branches on the basis of the house-keeping genes (Fig. 4). The other three strains (D3, D4 and E5) were cluster to the same clade with high similarities. Then the five house-keeping genes were concatenated for the MLSA analysis. The topology of the MLSA tree was similar to most of the single house-keeping gene trees (Fig. A2). The MLSA similarities ranged from 86.9% to 100%, with a mean value of 94.0%. The similarities of Strains C3, C4 and C5 ranged from 97.1%–97.3%, which were less than or equal to the soft species threshold (Liu et al., 2017). Strains D3, D4 and E5 were the same species and Strains C3, C4 and C5 would be different species belonging to genus Thioclava.
3.3 Oil degradation rates of the bacterial consortia and isolates
An oil-degrading test was performed within two weeks with the crude oil as the sole carbon resource. All the four consortia apparently showed good degrading ability, like emulsifying and turning brown, with no floating oil visible on the medium surface. The degradation rate was evaluated by gravity method (Fig. 5a). Consortia A and C both showed degradation rates of around 20% (24% and 22%, respectively) while Consortia D and E both showed similar higher rates around 40% (49% and 46%, respectively; Fig. 5a).
Furthermore, nine of the isolates with different 16S rRNA gene sequences were selected for degradation analysis. The degrading rates of the isolates varied widely (Fig. 5b). Three strains exhibited low degrading abilities (<15%), which were lower than those of the consortia in which they were found. The other six strains showed degradation rates of 25.8%–40.3%. Strain C3 showed the highest degradation rate (40.3%) among all screened bacteria.
3.4 Degradation of different oil components
Similar to the results of gravimetric method, the degradation rates of four strains (A3, A4, C1 and C2) were below 40% on alkanes (two weeks at 25°C; Fig. 6). The other five strains present much higher degrading ability. The degrading rates were very close to each other, ranging from 50.1% to 63.0%. Strain D2 showed the highest degrading ability. Most strains did not differ from each other in degradation of short-chain (<C15) alkanes. Strains A3, A4, C1 and C2 showed much lower degrading ability in different n-alkanes. Strains C3, D2, D4, E1 and E4 which showed good degrading ability in total alkanes were mainly degrading the 15–29 carbon atom alkanes (Table A3). Strain C3 exhibited broader degradation ability, affecting chain lengths from C15 to C39. The utilization rate of the alkane from C15 to C29 (except C16) ranged from 51.7% to 82.3%, and the degrading rate of C15 was especially higher than 80%. The middle-chain (C15 to C25 except C16, higher than 60%) alkane utilization of Strain D2 was higher than Strain C3.
The isolated strains showed much lower degrading abilities to degrade PAHs than the n-alkanes. Most of the bacteria show very low ability in PAHs degradation, with only Strain D2 showing a PAHs degrading rate above 40% (Fig. 6). Most strains were markedly less able to degrade PAHs than n-alkanes, especially Strains D4 and E4, which degraded less than 30% of the PAHs (Table A4). Strain D2 degraded the broadest range of PAHs, affecting all compounds examined (22 PAH compounds, two- to four-ring PAHs), with degrading rates of 34.9%–77.5%.
The degrading potential of the nine isolates was determined with seven types of carbon source (Table A5). Hexadecane and Dotriacontane represent middle chain and long chain alkanes, respectively. The other five carbon sources represent the PAHs with different rings. Strains A4 and E4 were found to have the ability to degrade Hexadecane and Dotriacontane. Strain D2 was able to utilize a variety of carbon sources and all the seven types of carbon source could be degraded.
4 Discussion
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In this study, we examined the bacterial characteristics of degradation in recently-spilled oil. The age of an oil spill likely played an important role in defining the bacterial diversity. Indeed, isolation of different strains has been shown to depend on succession within the sampled bacterial community (Atlas et al., 2015; Dubinsky et al., 2013; Mishamandani et al., 2016). Until now, most samples of bacterial communities associated with oil spills had been obtained at least 10 d after the spill (Kostka et al., 2011; Ruberto et al., 2003; Thomas et al., 2014). Functional consortia, with the potential to be utilized in bioremediation of oil spills, would exhibit substantial successional changes within this period (Dubinsky et al., 2013). Thus, strains of Alcanivorax, Marinobacter, Pseudomonas, Roseovarius, Thalassospira, Thioclava, etc. had been studied the ability of oil-degradation (Bacosa et al., 2015; Chronopoulou et al., 2015; Liu et al., 2007; Wang et al., 2014). Here, we collected oil-contaminated sediments 7 d after the oil-spill. Accordingly, we found several differences, including isolating the potentially novel strain Thioclava sp. C3. The strain belonging to Catenococcus was found to be the first time as an oil-degrading bacteria. Whereas previously isolated strains showed a good ability to degrade both alkanes and PAHs (Gao et al., 2015), most strains isolated here (except D2) degraded alkanes well, but not PAHs. This suggested that alkane-degrading bacteria, particularly obligate alkane degraders, were most easily isolated from freshly oil-polluted samples.
Bioaugmentation contributed importantly to the biodegradation of hydrocarbon contaminants in oil polluted environment (Ruberto et al., 2003; Simons et al., 2013). To improve the biodegrading efficiency, studies of suitable oil-degrading strains focused on isolating bacteria that showed high degradation efficiency. However, this approach ignored the potential of environmental factors in limiting degrading efficiency (Boopathy, 2000). The dominant bacteria were least limited to the environment. The predominant microorganisms with high oil-degrading ability would exhibit their ecological functions (Hazen et al., 2016). Using both high-throughput sequencing and 16S rRNA sequences from isolated strains, we found that Proteobacteria were the dominant bacterial phylum, in keeping with many previous studies (Hassanshahian et al., 2012; Hazen et al., 2010; King et al., 2015). Genus belonging to Alcanivoracaceae was a dominant genus at two of four sampling sites. The 16S rRNA gene sequence of Strain E4 was aligned with the representative OUT sequence of the dominant consortia. It showed a 99.56% similarity between the two sequences (Fig. A3). This means that Strain E4 was one of the most dominant strains in Consortium E. This research confirmed that the dominant strains could be discovered by the direction of the consortia structural analysis. This isolation method would provide time-saving way to screen dominant bacteria with high oil-degrading ability. Hence, Strain E4 might be more useful in field applications. This hypothesis could productively be investigated in future research.
5 Conclusions
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The current study investigated the enriched oil-degrading consortia via high-throughput sequencing, and the isolation procedure was also performed in the same enrichment. We found that the obligate alkane degraders were most easily isolated from freshly oil-polluted samples. Strain C3 would be a novel strain according to the low similarity to the type strain (98.37%). Alcanivorax borkumensis SK2 was one of the dominant taxon in Consortium E. Under the direction of the sequencing analysis, Strain E4 should be the dominant strain with high oil-degrading ability. Strain E4 was deposited in China General Microbiological Culture Collection Center with the number CGMCC 1.16160.
Funding
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  • The National Natural Science Foundation of China under contract Nos 41406127 and 41476103; the Basic Scientific Fund for National Public Research Institutes of China under contract No. 2015T05; the National Natural Science Foundation of China-Shandong Joint Funded Project under contract No. U1406403; the Marine Science and Technology Project of Huangdao District under contract No. 2014-4-20; the 2012 Taishan Scholar Award and China-ASEAN Maritime Cooperation Fund East Asia Marine Cooperation Platform.
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Article Info
doi: 10.1007/s13131-019-1353-2
  • Receive Date：2018-02-02
  • Online Date：2026-04-01
  • Published：2019-06-25
Article Data
Affiliations
History
  • Received：2018-02-02
  • Accepted：2018-03-22
Funding
The National Natural Science Foundation of China under contract Nos 41406127 and 41476103; the Basic Scientific Fund for National Public Research Institutes of China under contract No. 2015T05; the National Natural Science Foundation of China-Shandong Joint Funded Project under contract No. U1406403; the Marine Science and Technology Project of Huangdao District under contract No. 2014-4-20; the 2012 Taishan Scholar Award and China-ASEAN Maritime Cooperation Fund East Asia Marine Cooperation Platform.
Affiliations
    1 College of Marine Life Sciences, Ocean University of China, Qingdao 266003, China
    2 Marine Ecology Research Center, First Institute of Oceanography, Ministry of Natural Resources, Qingdao 266061, China
    3 National Deep Sea Center, Qingdao 266237, China
    4 College of Environmental Science and Engineering, Ocean University of China, Qingdao 266100, China
    5 Key Laboratory of Marine Chemical Theory and Technology, Ministry of Education, Qingdao 266100, China
    6 Laboratory for Marine Ecology and Environmental Science, Pilot National Laboratory for Marine Science and Technology (Qingdao), Qingdao 266237, China

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表12种不同金属材料的力学参数
科
Family		 属数
Number of
genus		 种数
Number of
species		 占总种数比例
Percentage of
total species (%)		 属
Genus		 种数
Number of
species		 占总种数比例
Percentage of total
species (%)
鹅膏菌科Amanitaceae 2 11 5.26 鹅膏菌属 Amanita 10 4.78
小菇科 Mycenaceae 2 12 5.74 丝盖伞属 Inocybe 5 2.39
多孔菌科 Polyporaceae 8 14 6.70 蜡蘑属 Laccaria 5 2.39
红菇科 Russulaceae 3 23 11.00 小皮伞属 Marasmius 6 2.87
小菇属 Mycena 11 5.26
光柄菇属 Pluteus 5 2.39
红菇属 Russula 17 8.13
栓菌属 Trametes 5 2.39
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