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Identification of three seagrass species in coral reef ecosystem by using multiple genes of DNA barcoding

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Abstract

Seagrasses constitute a significant part of coral reef ecosystems, representing high primary productivity and one of the most important coastal habitats in marine ecosystems. Though seagrasses possess irreplaceable ecological services to the marine environment, taxonomical ambiguity still exists due to similar morphological characters and phenotypic plasticity. As an emerging technology, DNA barcoding can effectively identify cryptic species using a short orthologous DNA region. In this study, we collected samples from five different locations (Daya Bay, Xincun Bay, Sanya Bay, Xisha Islands, and Nansha Islands), and three seagrass species Cymodocea rotundata, Thalassia hemprichii and Halophila ovalis was evaluated. Moreover, ITS, matK and rbcL genes were used as DNA barcodes. The results indicated that single ITS and concatenated ITS/matK/rbcL both conducted better species resolution than single matK and rbcL. Nevertheless, single ITS was more convenient. Furthermore, in all the four topology trees, three species resolved as 3 clusters as well H. ovalis and T. hemprichii grouped as sister clade. In the meantime, differentiation lay in intra-species based on the result of single ITS and three-locus analysis. Within H. ovalis and T. hemprichii separately, individuals from Xisha Islands first group together, then grouped with individuals from Nansha Islands and/or Xincun Bay and/or Sanya Bay and/or Daya Bay, which indicated that geographical distribution influenced population evolution. However, intra-species differentiation did not emerge in the tree of matK or rbcL.

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References

  • Ackerman JD (2006) Sexual reproduction of seagrasses. In: Larkum AWD, Orth RJ, Duarte CM (Eds.) Seagrasses: Biology, ecology and conservation. Springer, The Netherlands, p 89109

    Google Scholar 

  • Beck MW, Heck KL, Able KW, Childers DL, Eggleston DB, Gillanders BM et al. (2001) The identification, conservation, and management of estuarine and marine nurseries for fish and invertebrates. BioScience 51:633–641

    Article  Google Scholar 

  • Bonanno G, Orlando-Bonaca M (2017) Trace elements in Mediterranean seagrasses: accumulation, tolerance and biomonitoring. A review Mar Pollut Bull 125:8–18

    Article  CAS  Google Scholar 

  • Bricker E, Waycott M, Calladine A, Zieman JC (2011) High connectivity across environmental gradients and implications for phenotypic plasticity in a marine plant. Mar Ecol Prog Ser 423:57–67

    Article  Google Scholar 

  • Burkholder JM, Tomasko DA, Touchette BW (2007) Seagrasses and eutrophication. J Exp Mar Biol Ecol 350:46–72

    Article  Google Scholar 

  • CBOL Plant Working Group (2009) A DNA barcode for land plants. Proc Natl Acad Sci U.S.A. 106:12794–12797

    Article  Google Scholar 

  • Chase MW, Cowan RS, Hollingsworth PM, van den Berg C, Madrinan S, Petersen G et al. (2007) A proposal for a standardised protocol to barcode all land plants. Taxon 56:295–299

    Article  Google Scholar 

  • Coyer JA, Hoarau G, Kuo J, Tronholm A, Veldsink J, Olsen JL (2013) Phylogeny and temporal divergence of the seagrass family Zosteraceae using one nuclear and three chloroplast loci. Syst Biodivers 11:271–284

    Article  Google Scholar 

  • Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9:772–772

    Article  CAS  Google Scholar 

  • de Boer WF (2007) Seagrass-sediment interactions, positive feedbacks and critical thresholds for occurrence: a review. Hydrobiologia 591:5–24

    Article  Google Scholar 

  • Den Hartog C (1970) The sea-grasses of the world. Amsterdam Publishing Company, North-Holland

  • Duffy JE (2006) Biodiversity and the functioning of seagrass ecosystems. Mar Ecol Prog Ser 311:233–250

    Article  Google Scholar 

  • Evans SM, Sinclair EA, Poore AGB, Steinberg PD, Kendrick GA, Verges A (2014) Genetic diversity in threatened Posidonia australis seagrass meadows. Conser Genet 15:717–728

    Article  Google Scholar 

  • Franks SJ (2009) Genetics, evolution, and conservation of Island plants. J Plant Biol 53:1–9

    Article  Google Scholar 

  • Ghosh S, Bankura B, Das M (2016) DNA Barcoding: a tool to assess and conserve Marine Biodiversity. Springer International Publishing Switzerland: 43–61

  • Halpern BS, Walbridge S, Selkoe KA, Kappel CV, Micheli F, D’Agrosa C et al. (2008) A global map of human impact on marine ecosystems. Science 319:948–952

    Article  CAS  Google Scholar 

  • Han Q, Liu D (2014) Macroalgae blooms and their effects on seagrass ecosystems. J Ocean Univ China 13:791–798

    Article  CAS  Google Scholar 

  • Harrison PG, Bigley RE (1982) The recent introduction of the seagrass zostera-japonica aschers and graebn to the Pacific Coast of North-America. Can J Fisher Aquat Sci 39:1642–1648

    Article  Google Scholar 

  • Hebert PDN, Cywinska A, Ball SL, DeWaard JR (2003) Biological identifications through DNA barcodes. Proc Biol Sci 270:313-321

  • Hemminga M, Duarte CM (2000) Seagrass Ecology. Cambridge University Press, Cambridge (United Kingdom)

    Book  Google Scholar 

  • Hendriks IE, Olsen YS, Ramajo L, Basso L, Steckbauer A, Moore TS et al. (2014) Photosynthetic activity buffers ocean acidification in seagrass meadows. Biogeosciences 11:333–346

    Article  Google Scholar 

  • Hollingsworth PM, Forrest LL, Spouge JL, Hajibabaei M, Ratnasingham S, van der Bank M et al. (2009) A DNA barcode for land plants. Proc Natl Acad Sci U.S.A. 106:12794–12797

  • Hosokawa S, Nakaoka M, Miyoshi E, Kuwae T (2015) Seed dispersal in the seagrass Zostera marina is mostly within the parent bed in a protected bay. Mar Ecol Prog Ser 523:41–56

    Article  Google Scholar 

  • Hughes AR, Stachowicz J J (2004) Genetic diversity enhances the resistance of a seagrass ecosystem to disturbance. Proc Natl Acad Sci U.S.A. 101:8998–9002

  • Jiang ZJ, Liu SL, Zhang JP, Zhao CY, Wu YC, Yu S et al. (2017) Newly discovered seagrass beds and their potential for blue carbon in the coastal seas of Hainan Island, South China Sea. Mar Pollut Bull 125:513–521

    Article  CAS  Google Scholar 

  • Kendrick GA, Waycott M, Carruthers TJB, Cambridge ML, Hovey R, Krauss SL et al. (2012) The central role of dispersal in the maintenance and persistence of seagrass populations. BioScience 62:56–65

    Article  Google Scholar 

  • Kilminster K, McMahon K, Waycott M, Kendrick GA, Scanes P, McKenzie L et al. (2015) Unravelling complexity in seagrass systems for management: Australia as a microcosm. Sci Total Environ 534:97–109

    Article  CAS  Google Scholar 

  • Kress WJ, Wurdack KJ, Zimmer E A, Weigt LA, Janzen DH (2005) Use of DNA barcodes to identify flowering plants. Proc Natl Acad Sci U.S.A. 102:8369-8374

  • Lai S, Gillis LG, Mueller C, Bouma TJ, Guest JR, Last KS et al. (2013) First experimental evidence of corals feeding on seagrass matter. Coral Reefs 32:1061–1064

    Article  Google Scholar 

  • Li DZ, Gao LM, Li HT, Wang H, Ge XJ, Liu JQ et al. (2011) Comparative analysis of a large dataset indicates that internal transcribed spacer (ITS) should be incorporated into the core barcode for seed plants. Proc Natl Acad Sci U.S.A. 108:19641–19646

    Article  CAS  Google Scholar 

  • Li Y, Song N, Li WT, Gao TX (2012) Population genetics of Zostera marina Linnaeus (Zosteraceae) based on AFLP analysis. Biochem Syst Ecol 44:216–223

    Article  CAS  Google Scholar 

  • Ling J, Lin X, Zhang Y, Zhou W, Yang Q, Lin L et al. (2018) Community composition and transcriptional activity of ammonia-oxidizing prokaryotes of seagrass Thalassia hemprichii in coral reef ecosystems. Front Microbiol 9:7

    Article  Google Scholar 

  • Lucas C, Thangaradjou T, Papenbrock J (2012) Development of a DNA barcoding system for seagrasses: successful but not simple. PLoS One 7:e29987

    Article  CAS  Google Scholar 

  • McMahon K, van Dijk KJ, Ruiz-Montoya L, Kendrick GA, Krauss SL, Waycott M et al. (2014) The movement ecology of seagrasses Proc Biol Sci 281:20140878

    Google Scholar 

  • Nguyen XV, Höfler S, Glasenapp Y, Thangaradjou T, Lucas C, Papenbrock J (2015) New insights into DNA barcoding of seagrasses. Syst Biodivers 13:496–508

    Article  Google Scholar 

  • Nguyen XV, Holzmeyer L, Papenbrock J (2013) New record of the seagrass species Halophila major (Zoll.) Miquel in Vietnam: evidence from leaf morphology and ITS analysis. Bot Mar 56:313–321

    Article  Google Scholar 

  • Nguyen XV, Thirunavukarassu T, Papenbrock J (2013) Genetic variation among Halophila ovalis (Hydrocharitaceae) and closely related seagrass species from the coast of Tamil Nadu, India — an AFLP fingerprint approach. Systematics and Biodiversity 11:467–476

    Article  Google Scholar 

  • Orth RJ, Carruthers TJB, Dennison WC, Duarte CM, Fourqurean JW, Heck KL et al. (2006) A global crisis for seagrass ecosystems. BioScience 56:987

    Article  Google Scholar 

  • Petersen G, Seberg O, Short FT, Fortes MD (2014) Complete genomic congruence but non-monophyly of Cymodocea (Cymodoceaceae), a small group of seagrasses. Taxon 63:3–8

    Article  Google Scholar 

  • Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Hohna S et al. (2012) MrBayes 3.2: Efficient bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61:539–542

    Article  Google Scholar 

  • Serrano O, Mateo MA, Duenas-Bohorquez A, Renom P, Lopez-Saez JA, Martinez Cortizas A (2011) The Posidonia oceanica marine sedimentary record: a Holocene archive of heavy metal pollution. Sci Total Environ 409:4831–4840

    Article  CAS  Google Scholar 

  • Short FT, Carruthers TIB, Dennison WC, Waycott M (2007) Global seagrass distribution and diversity: a bioregional mode. J Exp Mar Biol Ecol 350:3–20

    Article  Google Scholar 

  • Short FT, Moore GE, Peyton KA (2010) Halophila ovalis in the Tropical Atlantic Ocean. Aquatic Botany 93:141–146

    Article  Google Scholar 

  • Short FT, Polidoro B, Livingstone SR, Carpenter K, Bandeira S, Bujang JS et al. (2011) Extinction risk assessment of the world’s seagrass species. Biol Conserv 144:1961–1971

    Article  Google Scholar 

  • Sinclair EA, Krauss SL, Anthony J, Hovey R, Kendrick GA (2014) The interaction of environment and genetic diversity within meadows of the seagrass Posidonia australis (Posidoniaceae). Mar Ecol Prog Ser 506:87–98

    Article  Google Scholar 

  • Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729

    Article  CAS  Google Scholar 

  • Tanaka N, Setoguchi H, Murata J (1997) Phylogeny of the family hydrocharitaceae inferred from rbcL and matK gene sequence data. J Plant Res. 110:329–337

    Article  CAS  Google Scholar 

  • Titlyanov EA, Titlyanova TV (2012) Marine plants in a coral reef ecosystem. Russ J Mar Biol 38:201–210

    Article  CAS  Google Scholar 

  • Travis SE, Sheridan P (2006) Genetic structure of natural and restored shoalgrass Halodule wrightii populations in the NW Gulf of Mexico. Mar Ecol Prog Ser 322:117–127

    Article  CAS  Google Scholar 

  • Uchimura M, Faye EJ, Shimada S, Inoue T, Nakamura Y (2008) A reassessment of Halophila species (Hydrocharitaceae) diversity with special reference to Japanese representatives. Bot Mar 51:258–268

    Article  Google Scholar 

  • Wang D, Wu Z, Chen C, Lan J, Wu R, Chen X, Zhang G, Li Y (2012) Distribution of seagrass resources and existing threat in Hainan Island. Mar. Environ. Sci. 31:34–38

    CAS  Google Scholar 

  • Ward RD, Zemlak TS, Innes BH, Last PR, Hebert PDN (2005) DNA barcoding Australia’s fish species. Philos Trans R Soc B Biol Sci 360:1847–1857

    Article  CAS  Google Scholar 

  • Waycott M (2000) Genetic factors in the conservation of seagrasses. Pac Conserv Biol 5:269–276

    Article  Google Scholar 

  • Waycott M, Duarte CM, Carruthers TJB, Orth RJ, Dennison WC, Olyarnik S et al (2009) Accelerating loss of seagrasses across the globe threatens coastal ecosystems. Proc Natl Acad Sci U.S.A. 106:12377–12381

  • Zhang X, Zhou Y, Xue DX, Liu JX (2016) Genetic divergence of the endangered seagrass Zostera japonica Ascherson & Graebner between temperate and subtropical coasts of China based on partial sequences of matK and ITS. Biochem Syst Ecol 68:51–57

    Article  Google Scholar 

  • Zheng F, Qiu G, Fan H, Zhang W(2013) Diversity, distribution and conservation of Chinese seagrass species. Biodiv Sci 21:517–526

    Google Scholar 

  • Zipperle AM, Coyer JA, Reise K, Stam WT, Olsen JL (2011) An evaluation of small-scale genetic diversity and the mating system in Zostera noltii on an intertidal sandflat in the Wadden Sea. Ann Bot 107:127–134

    Article  CAS  Google Scholar 

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Acknowledgements

The authors would like to thank all of the members of the Tropical Marine Biological Research Station in Hainan for their helping work in sample collecting.

Funding

The research was supported by the National Natural Science Foundation of China (41676163, 41276114), Strategic Priority Research Program of the Chinese Academy of Sciences (XDA13020300), Key Special Project for Introduced Talents Team of Southern Marine Science and Engineering Guangdong Laboratory (GML2019ZD0402), Innovation Academy of South China Sea Ecology and Environmental Engineering, Chinese Academy of Sciences (ISEE2018ZD02), National Key Research and Development Program of China (2017YFC0506301, 2018YFC1406505, 2018FY100105), Guangdong Province Public Welfare Research and Capacity Building Project (2015A020216016), Pearl River S&T Nova Program of Guangzhou (201806010017), and Science and Technology Planning Project of Guangdong Province, China (2020B1212060058).

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Authors and Affiliations

  1. CAS Key Laboratory of Tropical Marine Bio-resources and Ecology, Guangdong Provincial Key Laboratory of Applied Marine Biology, South China Sea Institute of Oceanology, Chinese Academy of Sciences, Guangzhou, 510301, China

    Xiancheng Lin, Junde Dong, Qingsong Yang, Weiguo Zhou, Ying Zhang, Manzoor Ahmad, Yingting Sun, Youshao Wang & Juan Ling

  2. University of Chinese Academy of Sciences, Beijing, 100049, China

    Xiancheng Lin, Qingsong Yang, Weiguo Zhou, Ying Zhang & Manzoor Ahmad

  3. Southern Marine Science and Engineering Guangdong Laboratory (Guangzhou), Guangzhou, 511458, China

    Junde Dong, Yingting Sun & Juan Ling

  4. Tropical Marine Biological Research Station in Hainan, Chinese Academy of Sciences and Hainan Key Laboratory of Tropical Marine Biotechnology, Sanya, 572000, China

    Junde Dong, Qingsong Yang, Weiguo Zhou & Juan Ling

  5. Guangdong Science and Technology Library (Guangdong Institute of Scientific and Technical Information and Development Strategy), Guangzhou, 510070, China

    Junde Dong & Yan Wang

  6. Innovation Academy of South China Sea Ecology and Environmental Engineering, Chinese Academy of Sciences, Guangzhou, 510301, China

    Qingsong Yang, Weiguo Zhou & Juan Ling

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  1. Xiancheng Lin
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  2. Junde Dong
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  10. Juan Ling
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Correspondence to Juan Ling.

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Lin, X., Dong, J., Yang, Q. et al. Identification of three seagrass species in coral reef ecosystem by using multiple genes of DNA barcoding. Ecotoxicology 30, 919–928 (2021). https://doi.org/10.1007/s10646-021-02397-3

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