Home Journals Articles Updates About
CN
image
收藏切换
Next-generation sequencing revealed specific microbial symbionts in Porites lutea with pigment abnormalities in North Sulawesi, Indonesia
收藏切换
PDF
Danyun OU1, Bin CHEN1, *, Tri Aryono HADI2, SUHARSONO2, Wentao NIU1, Yustian Rovi ALFIANSAH2
Acta Oceanologica Sinica | 2018, 37(12) : 78 - 84
Less
收藏切换
Acta Oceanologica Sinica | 2018, 37(12): 78-84
• Coastal Environment and Biodiversity in North Sulawesi, Indonesia •
Next-generation sequencing revealed specific microbial symbionts in Porites lutea with pigment abnormalities in North Sulawesi, Indonesia
Full
Danyun OU1, Bin CHEN1, *, Tri Aryono HADI2, SUHARSONO2, Wentao NIU1, Yustian Rovi ALFIANSAH2
Affiliations
  • 1 Third Institute of Oceanography, Ministry of Natural Resources, Xiamen 361005, China
  • 2 Research Center for Oceanography, Indonesian Institute of Sciences, Jakarta 14430, Indonesia
Published: 2018-12-25 doi: 10.1007/s13131-018-1291-4
Outline
收藏切换

Bacterial diseases affecting corals pose an enormous threat to the health of coral reefs. The relationship between certain bacterial species and coral diseases remain largely unknown. Pigment abnormalities are common in Porites lutea. Here we used Illumina 16S rRNA gene sequencing to analyze the bacterial communities associated with healthy P. lutea and P. lutea with pigment abnormalities. We observed an increase of alpha diversity of the bacterial community of P. lutea with pigment abnormalities, relative to healthy corals. We then identified changes in the abundance of individual operational taxonomic units (OTUs) between pigmented and healthy corals. We were able to identify eight OTUs associated with pigment abnormalities, which are possibly the causative agents of pigment abnormalities.

Porites lutea  /  pigment abnormalities  /  next-generation sequencing  /  16S rRNA  /  bacterial diversity
Danyun OU, Bin CHEN, Tri Aryono HADI, SUHARSONO, Wentao NIU, Yustian Rovi ALFIANSAH. Next-generation sequencing revealed specific microbial symbionts in Porites lutea with pigment abnormalities in North Sulawesi, Indonesia[J]. Acta Oceanologica Sinica, 2018 , 37 (12) : 78 -84 . DOI: 10.1007/s13131-018-1291-4
Full Text
Less
1 Introduction
Less
Microbial symbionts are versatile organisms aiding in the development and health of their host (Neish, 2009; Webster and Taylor, 2012). The interaction of corals and microbes is a fundamental aspect in the dynamics on reefs (Bourne et al., 2009). Corals continuously face changing environmental conditions, both on local and global scales (Bourne et al., 2009; Wegley et al., 2007).
Some bacterial species are reportedly responsible for coral diseases (Ben-Haim et al., 2003; Cervino et al., 2004; Kushmaro et al., 2001). The identification of bacterial pathogens associated with specific coral diseases is not easy, because the causing pathogens should be isolated and confirmed to fulfill Kohl’s law (Sussman, 2009). Six pathogens have been identified as causative agents for five kinds of coral diseases.
Culture-independent techniques, based on the characterization of symbiotic microorganisms associated with corals, have been used to gain a better understanding of symbiotic interactions (Morrow et al., 2012), and of the health conditions of coral systems (De Castro et al., 2010; Salipante et al., 2013).
Porites is a stony coral genus that is an accurate recorder of past marine surface conditions (Lough, 2010; Suzuki et al., 2000). Porites is thought to be the holobiont of bacterial pathogens, and to be easily affected by environmental stressors (Raymundo et al., 2005; Thurber et al., 2008). Pigment abnormalities are considered an inflammatory response of corals; however, the relationship between pigment abnormalities and bacterial communities remain unclear (Benzoni et al., 2010).
To illustrate the relationship between specific microbial communities and the pigment abnormalities in P. lutea, we analyzed the symbiotic microbial community of P. lutea with pigment abnormalities, and compared it with the microbial communities of healthy P. lutea.
2 Materials and methods
Less
2.1 Sample collection
Coral samples were collected during a Sino-Indonesia co-survey in late April to early May in 2013 at the Lembeh Strait. Samples of corals with pigment abnormalities, and of healthy corals, were collected at Site S5 located at the middle of the Lembeh Strait (1°27′13.6″N, 125°14′12.8″E, North Sulawesi, Indonesia) (Fig. 1). Coral samples were cut on site to collect separately pink segments and healthy segments (Fig. 2), and then fixed with 95% ethanol. Three parallels from pink segments and healthy segments respectively were subsampled for DNA analysis.
2.2 DNA extraction, amplification, and sequencing
Total genomic DNA was extracted from samples using the MP FastDNA Spin kit for Soil (MP Biomedicals). DNA concentration and purity were monitored on 1% agarose gels. DNA was diluted to 1 ng/μL in sterile water. The regions V3–V4 from the 16S gene were amplified using the specific primer 515F-806R with the barcode designed for the following sequencing. PCR reactions were carried out in 30 μL containing 15 μL of Phusion® High-Fidelity PCR Master Mix (New England Biolabs), 0.2 μmol/L of forward and reverse primers, and approximately 10 ng template DNA. Thermal cycling consisted of an initial denaturation step at 98°C for 1 min, followed by 30 cycles of denaturation at 98°C or for 10 s, annealing at 50°C for 30 s, and elongation at 72°C for 60 s, plus a final elongation step at 72°C for 5 min. Mix same volume of 1× loading buffer (contained SYB green) with PCR products and operate electrophoresis on 2% agarose gel for detection, and samples containing a band of 400–450 bp were selected for further experiments. PCR products were mixed in equal ratios. Then, the PCR products were purified using the GeneJET Gel Extraction Kit (Thermo Scientific). Sequencing libraries were generated using NEB Next® Ultra™ DNA Library Prep Kit for Illumina (NEB), following the manufacturer’s recommendations. The library quality was assessed using the Qubit@2.0 Fluorometer (Thermo Scientific) and the Agilent Bioanalyzer 2100 system. Finally, the library was sequenced on an Illumina MiSeq platform, generating 250–300 bp paired-end reads.
2.3 Data analysis
High-throughput sequencing data were processed using the Mothur software, as described in the pipeline of “Costello stool analysis” (Costello et al., 2009). In order to obtain more accurate sequences, sequences that were shorter than 400 bp, or that contained more than six polymers, were eliminated. Sequencing errors corresponding to artifacts of the sequencing process were reduced through the “denoising” algorithm (Reeder and Knight, 2010). After screening, filtering, and pre-clustering, unique sequences were checked for chimeras using Vsearch (Rognes et al., 2016). The qualified sequences were aligned with the reference set in the SILVA SSURef database Release 123 (Pruesse et al., 2007). Sequencing data were subsampled to eliminate the deviation due to the difference of sequence numbers across samples. After achieving an even number of sequences across samples, optimized reads were taxonomically assigned using the RDP-classifier with a bootstrap cut-off of 97% (Wang et al., 2007).
Observed richness, Simpson diversity, and the Shannon–Wiener index were measured based on the frequency of operational taxonomic units (OTUs) and genera in the assigned sequence collections after rare sequences were removed (Hill et al., 2003). Rarefaction curves were computed after discarding singletons. Beta diversity was estimated by computing weighted and unweighted UniFrac distances between samples using QIIME (Caporaso et al., 2010). Correlation analysis between the symbiotic bacterial communities of the samples were carried out using the statistical R package commond cor.test (Liu et al., 2014).
3 Results
Less
3.1 Diversity and richness of total symbiotic bacteria
A total of 439 734 sequences from six samples were recovered after Miseq sequencing. After sequence screening, filtering, pre-clustering and removal of chimeras, 425 182 qualified sequences were retained for alignment and OTU classification (these sequences accounted for 96.69% of the total raw sequences). In total 245 333 sequences representing bacterial taxons (16 951 to 98 768 sequences per sample) were recovered from these qualified sequences. As shown in the rarefaction curve based on the bacterial OTU number, the sequencing data can reflect the diversity and richness of the bacterial community of the coral samples, because all the curves reached the near plateau phase (Fig. 3). Additionally, the coverage value shown in Table 1 also indicated that pyro-sequencing data covered 89.39%–96.95% of the bacterial community in the coral samples.
The bacterial community in P. lutea with pigment abnormalities had features differing from those of healthy P. lutea. The relative diversity of the bacterial community from P. lutea with pigment abnormalities was higher than that from healthy coral samples, as indicated by the Shannon index. The Shannon’s index showed different patterns; it increased as the sequence number increased in the samples of P. lutea with pigment abnormalities, while in healthy corals the Shannon’s index decreased as the sequence number increased. The Simpson’s index in the samples of P. lutea with pigment abnormalities was higher than that of healthy corals, which also indicates that the bacterial community in P. lutea with pigment abnormalities is more diverse than in healthy corals. The community richness represented by Chao’s index and sobs showed that the bacterial community in P. lutea with pigment abnormalities has higher richness than healthy corals (Table 1).
3.2 Bacterial community composition
A total of 16 951 sequences from each sample were clustered into 8 007 OTUs at a similarity of 97%, using the furthest neighbor algorithm by Vsearch. Bray-Curtis distance matrix, based on the correlation analysis of the six samples, indicated that the symbiotic bacterial community structure in P. lutea with pigment abnormalities and in healthy corals were different from each other, while those in the three parallels of each group were quite similar (Fig. 4).
From the 8 007 OTUs clustered using Mothur, 7 943 OTUs were classified by blasting against NCBI microbial 16S rRNA database. After removing rare OTUs, 936 qualified OTUs accounted for the 15 335–16 049 sequences that were finally recovered. The most abundant bacteria phyla, as calculated by the size (number of sequences) of the phylum of each sample, were Proteobacteria (58.47% of the total), Actinobacteria (19.49% of the total) and Chlorobi (14.18% of the total). Proteobacteria was the most versatile phylum, accounting for 3 449–10 022 and 10 114–12 767 of the sequences in healthy corals, and in P. lutea with pigment abnormalities, respectively.
A total of 399 genera of symbiotic bacteria in healthy P. lutea and in P. lutea with pigment abnormalities were identified by OTU analysis. Bacteria belonging to the 20 most abundant genera constituted more than 77% of the total identified bacteria in P. lutea (77.30% of the total in healthy P. lutea, and 78.09% in P. lutea with pigment abnormalities). The five most abundant genera, Vibrio, Prosthecochloris, Blastococcus, Roseibium and Pseudoalteromonas accounted for 16.21%, 14.18%, 10.06%, 6.25% and 3.77% of the total sequences, respectively. Among these genera, the most abundant OTUs of symbiotic bacteria were Vibrio (0.97%–8.33% in healthy P. lutea and 16.89%–34.57% in P. lutea with pigment abnormalities), Prosthecochloris (0.20%–61.69% in healthy P. lutea and 0.45%–8.67% in P. lutea with pigment abnormalities), Blastococcus (4.66%–19.69% in healthy P. lutea and 4.17%–11.33% in P. lutea with pigment abnormalities), Roseibium (2.19%–8.77% in healthy P. lutea and 5.55%–9.73% in P. lutea with pigment abnormalities), and Pseudoalteromonas (0.90%–2.32% in healthy P. lutea and 4.89%–8.63% in P. lutea with pigment abnormalities) (Fig. 5). Vibrio species in P. lutea with pigment abnormalities (16.21%) were significantly more abundant than in healthy P. lutea (4.94%), which suggests that Vibrio might play an important role in the pigment development in P. lutea.
According to Silva 16S rRNA database, and after removing rare OTUs, a total of 936 bacterial OTUs belonging to 575 species were recovered from subsampled healthy P. lutea and P. lutea with pigment abnormalities. Vibrio, Photobacterium, Acinetobacter, Mesorhizobium and Desulfovibrio were most versatile bacteria genus with 24, 9, 7, 6, and 5 species, respectively (Appendix Table A1). After comparing the 22 most abundant bacterial OTUs (with abundance over 1% of the total OTUs) of healthy P. lutea and P. lutea with pigment abnormalities, we identified 2 OTUs consistently associated with P. lutea with pigment abnormalities, and 8 OTUs consistently associated with healthy P. lutea (Fig. 6). OTUs associated with healthy P. lutea were Prothecochloris vibrioformis and Prothecochloris aestuarii. OTUs associated with P. lutea with pigment abnormalities were Vibrio hyugaensis, Vibrio fortis, Roseibium aquae, Pseudoalteromonas arabiensis, Oscillochloris trichoides, Kofleria flava, Photobacterium gaetbulicola and Vibrio xuii, with 12.80%, 10.58%, 6.30%, 4.93%, 3.25%, 2.26%, 1.98% and 1.90% of the pigmented group versus 1.95%, 1.85%, 2.05 %, 1.34%, 0.66%, 0.67%, 0.27% and 0.31% of the healthy group (Fig. 6). Among these, six OTUs associated with P. lutea with pigment abnormalities were related to bacterial families that include known coral pathogens (Vibrionaceae), to symbiotic bacteria found in diseased marine invertebrates (Rhodobacteraceae), or to algicidal bacteria (Pseudoalteromonadaceae) (Sunagawa et al., 2009).
4 Discussion
Less
The symbiotic bacterial community changed drastically in P. lutea with pigment abnormalities, exhibiting an increase in hundreds of OTUs, relative to healthy P. lutea. This change was evidenced by increased bacterial diversity and richness, which is consistent with other coral diseases (Pantos et al., 2003; Séré et al., 2013; Sunagawa et al., 2009).
Proteobacteria was the most abundant phylum in the symbiotic bacterial OTUs, which is in keeping with previous 16S rDNA and metagenomic analysis of bacteria associated with Porites (Rohwer et al., 2002; Wegley et al., 2007). The other two most abundant phyla were Actinobacteria and Chlorobi, which were different to those reported in previous studies, in which Firmicutes and Actinobacteria were the second and third most abundant phyla (Rohwer et al., 2002; Wegley et al., 2007).
The five most abundant genera, Vibrio, Prosthecochloris, Blastococcus, Roseibium and Pseudoalteromonas accounted for more than 50% of the total sequences found in P. lutea. These results are similar to previous reports which suggested that Vibrio and Pseudoalteromonas were the most abundant bacterial genera in P. lutea from southern Hainan Island in China. It is thus likely that these genera form a part of the natural microbiota of P. lutea (Li et al., 2014). Furthermore, Vibrio were more abundant in P. lutea with pigment abnormalities than in healthy P. lutea, indicating that Vibrio might be involved in the etiology of the pigment abnormalities of P. lutea.
Several Vibrio species are well-known pathogens of marine shrimp, fish, invertebrates and coral (Austin et al., 2005; Ben-Haim and Rosenberg, 2002; Kushmaro et al., 1997). Vibrio Shiloi, the first coral pathogen to be identified, is an etiological agent of bleaching of the coral Oculina patagonica (Kushmaro et al., 1996; 2001). Vibrio coralliilyticus is an etiological agent of bleaching of the coral Pocillopora damicornis (Ben-Haim et al., 2003). Four Vibrio species are related to yellow blotch/band disease of the coral Montastrea spp. (Cervino et al., 2004). In our research, three Vibrio species, Vibrio hyugaensis, Vibrio fortis, and Vibrio xuii accounted more than 25% of the total microbial OTUs in P. lutea with pigment abnormalities, which suggested these Vibrio species may be involved in the development of pigment abnormalities.
Acknowledgements
Less
The authors thank Bai Renao for contributing to DNA extraction, and Novogene Ltd. for helping with Illumina DNA sequencing.
Funding
Less
  • The China-Indonesia Maritime Cooperation Fund Project “China-Indonesia Bitung Ecological Station Establishment”; the National Natural Science Foundation of China under contract No. 41506180; the Public Science and Technology Research Funds Projects of Ocean under contract No. 201505009.
References
Less
Austin B, Austin D, Sutherland R, et al. 2005. Pathogenicity of vibrios to rainbow trout (Oncorhynchus mykiss, Walbaum) and Artemia nauplii. Environmental Microbiology, 7(9): 1488–1495, doi: 10.1111/emi.2005.7.issue-9
Ben-Haim Y, Rosenberg E. 2002. A novel Vibrio sp.pathogen of the coral Pocillopora damicornis. Marine Biology, 141(1): 47–55, doi: 10.1007/s00227-002-0797-6
Ben-Haim Y, Zicherman-Keren M, Rosenberg E. 2003. Temperature-regulated bleaching and lysis of the coral Pocillopora damicornis by the novel pathogen Vibrio coralliilyticus. Applied and Environmental Microbiology, 69(7): 4236–4242, doi: 10.1128/AEM.69.7.4236-4242.2003
Benzoni F, Galli P, Pichon M. 2010. Pink spots on Porites: not always a coral disease. Coral Reefs, 29(1): 153, doi: 10.1007/s00338-009-0571-z
Bourne D G, Garren M, Work T M, et al. 2009. Microbial disease and the coral holobiont. Trends in Microbiology, 17(12): 554–562, doi: 10.1016/j.tim.2009.09.004
Caporaso J G, Kuczynski J, Stombaugh J, et al. 2010. QIIME allows analysis of high-throughput community sequencing data. Nature Methods, 7(5): 335–336, doi: 10.1038/nmeth.f.303
Cervino J M, Hayes R L, Polson S W, et al. 2004. Relationship of Vibrio species infection and elevated temperatures to yellow blotch/band disease in Caribbean corals. Applied and Environmental Microbiology, 70(11): 6855–6864, doi: 10.1128/AEM.70.11.6855-6864.2004
Costello E K, Lauber C L, Hamady M, et al. 2009. Bacterial community variation in human body habitats across space and time. Science, 326(5960): 1694–1697, doi: 10.1126/science.1177486
De Castro A P, Araújo Jr S D, Reis A M M, et al. 2010. Bacterial community associated with healthy and diseased reef coral Mussismilia hispida from eastern Brazil. Microbial Ecology, 59(4): 658–667, doi: 10.1007/s00248-010-9646-1
Hill T C J, Walsh K A, Harris J A, et al. 2003. Using ecological diversity measures with bacterial communities. FEMS Microbiology Ecology, 43(1): 1–11, doi: 10.1111/fem.2003.43.issue-1
Kushmaro A, Banin E, Loya Y, et al. 2001. Vibrio shiloi sp.nov., the causative agent of bleaching of the coral Oculina patagonica. International Journal of Systematic and Evolutionary Microbiology, 51(4): 1383–1388, doi: 10.1099/00207713-51-4-1383
Kushmaro A, Loya Y, Fine M, et al. 1996. Bacterial infection and coral bleaching. Nature, 380(6573): 396
Kushmaro A, Rosenberg E, Fine M, et al. 1997. Bleaching of the coral Oculina patagonica by Vibrio AK-1. Marine Ecology Progress Series, 147: 159–165, doi: 10.3354/meps147159
Li Jie, Chen Qi, Long Lijuan, et al. 2014. Bacterial dynamics within the mucus, tissue and skeleton of the coral Porites lutea during different seasons. Scientific Reports, 4: 7320
Liu Yang, Yao Su, Xu Pengpeng, et al. 2014. Composition and diversity of endophytic bacterial communities in Noni (Morinda citrifolia L.) seeds. International Journal of Agricultural Policy and Research, 2(3): 98–104
Lough J M. 2010. Climate records from corals. WIREs Climate Change, 1(3): 318–331, doi: 10.1002/wcc.39
Morrow K M, Moss A G, Chadwick N E, et al. 2012. Bacterial associates of two Caribbean coral species reveal species-specific distribution and geographic variability. Applied and Environmental Microbiology, 78(18): 6438–6449, doi: 10.1128/AEM.01162-12
Neish A S. 2009. Microbes in gastrointestinal health and disease. Gastroenterology, 136(1): 65–80, doi: 10.1053/j.gastro.2008.10.080
Pantos O, Cooney R P, Le Tissier M D A, et al. 2003. The bacterial ecology of a plague-like disease affecting the Caribbean coral Montastrea annularis. Environmental Microbiology, 5(5): 370–382, doi: 10.1046/j.1462-2920.2003.00427.x
Pruesse E, Quast C, Knittel K, et al. 2007. SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Research, 35(21): 7188–7196, doi: 10.1093/nar/gkm864
Raymundo L J, Rosell K B, Reboton C T, et al. 2005. Coral diseases on Philippine reefs: genus Porites is a dominant host. Diseases of Aquatic Organisms, 64(3): 181–191
Reeder J, Knight R. 2010. Rapidly denoising pyrosequencing amplicon reads by exploiting rank-abundance distributions. Nature Methods, 7(9): 668–669
Rognes T, Flouri T, Nichols B, et al. 2016. VSEARCH: a versatile open source tool for metagenomics. PeerJ, 4(17): e2584
Rohwer F, Seguritan V, Azam F, et al. 2002. Diversity and distribution of coral-associated bacteria. Marine Ecology Progress Series, 243: 1–10, doi: 10.3354/meps243001
Séré M G, Tortosa P, Chabanet P, et al. 2013. Bacterial communities associated with Porites white patch syndrome (PWPS) on three western Indian Ocean (WIO) coral reefs. PLoS One, 8(12): e83746, doi: 10.1371/journal.pone.0083746
Salipante S J, Sengupta D J, Rosenthal C, et al. 2013. Rapid 16S rRNA next-generation sequencing of polymicrobial clinical samples for diagnosis of complex bacterial infections. PLoS One, 8(5): e65226, doi: 10.1371/journal.pone.0065226
Sunagawa S, DeSantis T Z, Piceno Y M, et al. 2009. Bacterial diversity and White Plague Disease-associated community changes in the Caribbean coral Montastraea faveolata. The ISME Journal, 3(5): 512–521, doi: 10.1038/ismej.2008.131
Sussman M. 2009. Coral disease pathogens of the Indo-Pacific Ocean [dissertation]. Townsville: James Cook University
Suzuki A, Kawahata H, Tanimoto Y, et al. 2000. Skeletal isotopic record of a Porites coral during the 1998 mass bleaching event. Geochemical Journal, 34(4): 321–329, doi: 10.2343/geochemj.34.321
Thurber R L V, Barott K L, Hall D, et al. 2008. Metagenomic analysis indicates that stressors induce production of herpes-like viruses in the coral Porites compressa. Proceedings of the National Academy of Sciences of the United States of America, 105(47): 18413–18418, doi: 10.1073/pnas.0808985105
Wang Qiong, Garrity G M, Tiedje J M, et al. 2007. Naïve Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Applied and Environmental Microbiology, 73(16): 5261–5267, doi: 10.1128/AEM.00062-07
Webster N S, Taylor M W. 2012. Marine sponges and their microbial symbionts: love and other relationships. Environmental Microbiology, 14(2): 335–346, doi: 10.1111/j.1462-2920.2011.02460.x
Wegley L, Edwards R, Rodriguez-Brito B, et al. 2007. Metagenomic analysis of the microbial community associated with the coral Porites astreoides. Environmental Microbiology, 9(11): 2707–2719, doi: 10.1111/emi.2007.9.issue-11
Appendix
Less
Year 2018 volume 37 Issue 12
PDF
30
16
Cite this Article
BibTeX
Article Info
doi: 10.1007/s13131-018-1291-4
  • Receive Date：2017-06-15
  • Online Date：2026-04-14
  • Published：2018-12-25
Article Data
Affiliations
History
  • Received：2017-06-15
  • Accepted：2018-03-15
Funding
The China-Indonesia Maritime Cooperation Fund Project “China-Indonesia Bitung Ecological Station Establishment”; the National Natural Science Foundation of China under contract No. 41506180; the Public Science and Technology Research Funds Projects of Ocean under contract No. 201505009.
Affiliations
    1 Third Institute of Oceanography, Ministry of Natural Resources, Xiamen 361005, China
    2 Research Center for Oceanography, Indonesian Institute of Sciences, Jakarta 14430, Indonesia

Corresponding:

References
Share
https://castjournals.cast.org.cn/joweb/aos/EN/10.1007/s13131-018-1291-4
Share to
QR

Scan QR to access full text

Cite this article
BibTeX
Citations
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
关闭全屏
  • BibTeX
  • EndNote
  • RefWorks
  • TxT
Links
Articles
Latest Articles
Most Read
Collections
Updates
Events
News
Multimedia
About
About Us
Contact
No. 86 Xueyuan South Road, Haidian District, Beijing
100081
010-62199257
qkjq@cast.org.cn

Copyright © 2025 China Association for Science and Technology. All rights reserved. For all open access content, the relevant licensing terms apply.
Sponsored by the Office of the Leading Group for Cybersecurity and Informatization of CAST, and supported by Science and Technology Review Publishing House