Monthly eDNA Monitoring of an Invasive Bryozoan, Bugulina californica, in Seawater Using Species-Specific Markers
Abstract
:Simple Summary
Abstract
1. Introduction
2. Materials and Methods
2.1. Field Survey and Specimen Morphological Examination
2.2. Molecular and Morphological Identification of B. californica
2.2.1. DNA Extraction, Amplification, and Sequencing
2.2.2. Molecular Identification
2.3. Species-Specific Primers and eDNA
2.3.1. Design and Validation of B. californica-Specific Primers and Probe
2.3.2. Collection and Isolation of eDNA
2.3.3. eDNA Detection
3. Results
3.1. Molecular Assay Design
3.1.1. Gene Selection for Designing Species-Specific Markers
3.1.2. Species-Specific Markers Design and Validation
3.2. Environmental DNA Monitoring
3.2.1. Detection of B. californica in Field and eDNA Samples
3.2.2. Calculation of B. californica DNA Copies
4. Discussion
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
Appendix A
Phylum | Class | Species | Accession Number |
---|---|---|---|
Porifera | Demospongiae | Amphimedon compressa | EU237474 |
Aplysina fulva | EU237476 | ||
Callyspongia plicifera | EU237477 | ||
Chondrilla nucula | EU237478 | ||
Halisarca dujardini | EU237483 | ||
Hippospongia lachne | EU237484 | ||
Igernella notabilis | EU237485 | ||
Iotrochota birotulata | EU237486 | ||
Plakinastrella onkodes | EU237487 | ||
Topsentia ophiraphidites | EU237482 | ||
Vaceletia sp. | EU237489 | ||
Xestospongia muta | EU237490 | ||
Cnidaria | Hydrozoa | Clava multicornis | JN700935, NC 016465 |
Craspedacusta sowerbyi | JN593332, NC 018537 | ||
Cubaia aphrodite | JN700942, NC 016467 | ||
Hydra magnipapillata | NC 011221 | ||
Hydra oligactis | EU237491, NC 010214 | ||
Hydra sinensis | JX089978, NC 021406 | ||
Hydra vulgaris | HM369413 | ||
Hydra vulgaris | HM369414 | ||
Laomedea flexuosa | JN700945, NC 016463 | ||
Turritopsis dohrnii | KT020766, KT899097, NC 031213 | ||
Scyphozoa | Aurelia aurita | DQ787873, HQ694729, NC 008446 | |
Aurelia sp. | LC005413, LC005414 | ||
Cassiopea frondosa | JN700936, NC 016466 | ||
Chrysaora quinquecirrha | HQ694730, NC 020459 | ||
Craspedacusta sowerbyi | JN593332 | ||
Haliclystus antarcticus | KU947038, NC 030337 | ||
Anthozoa | Alveopora allingi | AB907079 | |
Alveopora catalai | AB907081 | ||
Alveopora excelsa | AB907085 | ||
Alveopora japonica | AB907087 | ||
Alveopora sp. | KJ634271 | ||
Alveopora spongiosa | AB907093 | ||
Alveopora tizardi | AB907096 | ||
Alveopora verrilliana | AB907097 | ||
Arthropoda | Hexanauplia | Acasta sulcata | KJ754818, NC 029168 |
Amphibalanus amphitrite | KF588709, NC 024525 | ||
Armatobalanus allium | KJ754817, NC 029167 | ||
Balanus balanus | KM660676, NC 026466 | ||
Capitulum mitella | AB167462 | ||
Chelonibia testudinaria | KJ754819, NC 029169 | ||
Chthamalus antennatus | KP294312, NC 026730 | ||
Epopella plicata | KM008743, NC 033393 | ||
Lepas anserifera | KP294311, NC 026576 | ||
Lepas australis | KM017964, NC 025295 | ||
Megabalanus ajax | KF501046, NC 024636 | ||
Megabalanus volcano | AB167539, NC 006293 | ||
Pollicipes mitella | AY514042 | ||
Pollicipes polymerus | AY456188, NC 005936 | ||
Striatobalanus amaryllis | KF493890, NC 024526 | ||
Tetraclita japonica | AB126701, NC 008974 | ||
Tetraclita serrata | KJ434948, NC 029154 | ||
Tetraclitella divisa | KJ754822, NC 029170 | ||
Bryozoa | Gymnolaemata | Bugula dentata | KC129718 |
Bugula flabellata | AY061749 | ||
Bugula fulva | KC129719 | ||
Bugula migottoi | KC129720 | ||
Bugula neritina | AY690838, KC129722, KC129735, KC129735, KC129754, KC129822 | ||
Bugula stolonifera | KC129849 | ||
Bugula turrita | KC129850 | ||
Celleporella hyalina | JQ839275, JQ839276, NC 018344 | ||
Flustra foliacea | JQ061319, NC 016722 | ||
Flustrellidra hispida | DQ157889, NC 008192 | ||
Membranipora grandicella | NC 018355 | ||
Tubulipora flabellaris | EU563937 | ||
Watersipora subtorquata | EU365892, NC 011820 | ||
Echinodermata | Crinoidea | Antedon mediterranea | AM404181, NC 010692 |
Florometra serratissima | NC 001878 | ||
Neogymnocrinus richeri | DQ068951, NC 007689 | ||
Phanogenia gracilis | DQ068952, NC 007690 | ||
Asteroidea | Acanthaster brevispinus | AB231476, NC 007789 | |
Acanthaster planci | AB231475, NC 007788 | ||
Aphelasterias japonica | NC 025766 | ||
Asterias amurensis | AB183559, NC 006665 | ||
Astropecten polyacanthus | AB183560, NC 006666 | ||
Luidia quinaria | AB183558 | ||
Patiria pectinifera | D16387 | ||
Ophiuroidea | Amphipholis squamata | FN562578, NC 013876 | |
Astrospartus mediterraneus | FN562580, NC 013878 | ||
Astrospartus mediterraneus | NC 013878 | ||
Ophiacantha linea | NC 023254 | ||
Ophiocomina nigra | FN562577, NC 013874 | ||
Ophiopholis aculeata | AF314589, NC 005334 | ||
Ophiura albida | AM404180, NC 010691 | ||
Ophiura lutkeni | AY184223, NC 005930 | ||
Echinoidea | Arbacia lixula | NC 001770 | |
Echinocardium cordatum | NC 013881 | ||
Heliocidaris crassispina | NC 023774 | ||
Hemicentrotus pulcherrimus | NC 023771 | ||
Loxechinus albus | JX888466 | ||
Mesocentrotus franciscanus | NC 024177 | ||
Mesocentrotus nudus | NC 020771 | ||
Nacospatangus alta | NC 023255 | ||
Paracentrotus lividus | J04815 | ||
Pseudocentrotus depressus | KC490913, NC 023773 | ||
Sterechinus neumayeri | NC 027063 | ||
Strongylocentrotus droebachiensis | EU054306, NC 009940 | ||
Strongylocentrotus intermedius | KC490912, NC 023772 | ||
Strongylocentrotus pallidus | NC 009941 | ||
Strongylocentrotus purpuratus | NC 001453 | ||
Temnopleurus hardwickii | NC 026200 | ||
Holothuroidea | Apostichopus japonicus | EU294194 | |
Balanoglossus clavigerus | NC 013877 | ||
Cucumaria miniata | AY182376 | ||
Holothuria forskali | NC 013884 | ||
Holothuria scabra | NC 027086 | ||
Parastichopus californicus | NC 026727 | ||
Parastichopus nigripunctatus | NC 013432 | ||
Parastichopus parvimensis | NC 029699 | ||
Peniagone sp. | KF915304 | ||
Stichopus horrens | HQ000092, NC 014454 | ||
Chordata | Ascidiacea | Aplidium conicum | FN313538, NC 013584 |
Aplidium tabarquensis | HF548555 | ||
Bugulina californica | HF548561, NC 021469 | ||
Botrylloides leachii | HF548553, HG931921, NC 024103 | ||
Botrylloides nigrum | HF548559, NC 021467 | ||
Botrylloides pizoni | HF548554, HG931922, NC 024104 | ||
Botrylloides violaceus | HF548552, NC 024256 | ||
Botryllus schlosseri | FM177702, HF548550, HF548551, HG931923, NC 021463 | ||
Ciona intestinalis | AJ517314, NC 004447 | ||
Ciona intestinalis type B | AM292218, NC 017929 | ||
Ciona savignyi | AB079784, NC 004570 | ||
Clavelina lepadiformis | AM292603, FJ839918, NC 012887 | ||
Clavelina phlegraea | AM292604, NC 024105 | ||
Didemnum vexillum | KM259616, KM259617, NC 026107 | ||
Diplosoma listerianum | FN313539, NC 013556 | ||
Halocynthia roretzi | AB024528, NC 002177 | ||
Halocynthia spinosa | HF548558, NC 021466 | ||
Herdmania momus | AM292602, FN296153, NC 013561 | ||
Microcosmus sulcatus | AM292321, NC 013752 | ||
Phallusia fumigata | NC 009834 | ||
Phallusia mammillata | AM292320, NC 009833 | ||
Polycarpa mytiligera | HF548556, NC 021464 | ||
Pyura gangelion | HF548557, NC 021465 | ||
Rhodosoma turcicum | HF548560, NC 021468 | ||
Styela clava | HG931920 | ||
Styela plicata | AM292601, NC 013565 |
Appendix B
1 | 2 | 3 | 4 | 5 | 6 | 7 | 8 | 9 | 10 | 11 | 12 | ||
---|---|---|---|---|---|---|---|---|---|---|---|---|---|
1 | Bugula flabellata AY633484 | 0.004 | 0.022 | 0.026 | 0.022 | 0.022 | 0.022 | 0.025 | 0.025 | 0.025 | 0.025 | 0.038 | |
2 | Bugula flabellata AY061749 | 0.008 | 0.022 | 0.025 | 0.022 | 0.022 | 0.022 | 0.024 | 0.024 | 0.024 | 0.024 | 0.038 | |
3 | Bugulina fulva KC129719 | 0.212 | 0.215 | 0.022 | 0.022 | 0.022 | 0.022 | 0.020 | 0.020 | 0.020 | 0.020 | 0.035 | |
4 | Bugula simplex AY633478 | 0.272 | 0.268 | 0.223 | 0.024 | 0.024 | 0.024 | 0.023 | 0.023 | 0.023 | 0.023 | 0.034 | |
5 | Bugula turbinata AY633480 | 0.225 | 0.220 | 0.208 | 0.233 | 0.003 | 0.002 | 0.021 | 0.021 | 0.021 | 0.021 | 0.032 | |
6 | Bugula turbinata AY633481 | 0.223 | 0.217 | 0.211 | 0.233 | 0.004 | 0.002 | 0.021 | 0.021 | 0.021 | 0.021 | 0.033 | |
7 | Bugula turbinata AY633482 | 0.223 | 0.217 | 0.211 | 0.230 | 0.002 | 0.002 | 0.020 | 0.020 | 0.020 | 0.020 | 0.033 | |
8 | Bugulina californica MZ209214 | 0.257 | 0.254 | 0.183 | 0.225 | 0.183 | 0.183 | 0.180 | 0.000 | 0.000 | 0.000 | 0.037 | |
9 | Bugulina californica voucher MZ217204 | 0.257 | 0.254 | 0.183 | 0.225 | 0.183 | 0.183 | 0.180 | 0.000 | 0.000 | 0.000 | 0.037 | |
10 | Bugulina californica MZ209213 | 0.257 | 0.254 | 0.183 | 0.225 | 0.183 | 0.183 | 0.180 | 0.000 | 0.000 | 0.000 | 0.037 | |
11 | Bugulina californica MZ209214 | 0.257 | 0.254 | 0.183 | 0.225 | 0.183 | 0.183 | 0.180 | 0.000 | 0.000 | 0.000 | 0.037 | |
12 | Terebratalia transversa FJ196085 | 0.449 | 0.453 | 0.409 | 0.404 | 0.369 | 0.366 | 0.365 | 0.433 | 0.433 | 0.433 | 0.433 |
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Number | Region | Location | Latitude | Longitude |
---|---|---|---|---|
1 | East Sea | Sokcho | 38°12′34.76″ N | 128°35′48.61″ E |
2 | Donghae | 37°29′21.30″ N | 129°07′23.35″ E | |
3 | Jukbyeon | 37°03′17.32″ N | 129°25′26.30″ E | |
4 | Yangpo | 35°52′56.34″ N | 129°31′35.13″ E | |
5 | Korea Strait | Busan | 35°07′02.60″ N | 129°02′55.49″ E |
6 | Tongyeong | 34°50′23.05″ N | 128°25′12.58″ E | |
7 | Yeosu | 34°44′31.11″ N | 127°45′20.08″ E | |
8 | Wando | 34°19′04.43″ N | 126°45′11.68″ E | |
9 | West Sea | Mokpo | 34°46′51.50″ N | 126°22′59.76″ E |
10 | Bieung | 35°56′11.21″ N | 126°31′38.01″ E | |
11 | Dangjin | 36°59′14.82″ N | 126°44′50.86″ E | |
12 | Incheon | 37°27′34.05″ N | 126°37′32.32″ E |
Primers and Probe | Sequences | Reference |
---|---|---|
LCO1490 | 5′-GGTCAACAAATCATAAAGATATTGG-3′ | Folmer et al. 1994 [38] |
HCO2198 | 5′-TAAACTTCAGGGTGACCAAAAAATCA-3′ | |
BuCa_SF | 5′-CTTTTACCACCTGCACTAGCT-3′ | Designed in this study |
BuCa_SR | 5′-GATGGTCCACTATGACCGAGA-3′ | |
BuCa Probe | 5′-6-Fam-TGAAAGAGGAGCAGGTACAGGATGA-BHQ-1-3′ |
Taxon | Location |
---|---|
Phylum BRYOZOA | |
Class Gymnolaemata | |
Bugulina californica | Gonghyeonjin |
Ulsan | |
Dadaepo | |
Bugula neritina | Ayajin |
Watersipora subtorquata | Jongdal |
Tricellaria occidentalis | Kimnyeong |
Schizoporella unicornis | Yangpo |
Jellyella tuberculata | Seoguipo |
Phylum CNIDARIA | |
Class Hydrozoa | |
Ectopleura crocea | Mulchi |
Bougainvillia ramosa | Incheon |
Phylum CHORDATA | |
Class Ascidiacea | |
Ascidiella aspersa | Chuksan |
Ciona robusta | Yangpo |
Phylum ECHINODERMATA | |
Class Crinoidea | |
Antedon serrata | Busan |
Heliometra glacialis | Daejin |
Class Asteroidea | |
Patiria pectinifera | Juckbyeon |
Asterias amurensis | Dadaepo |
Class Ophiuroidea | |
Ophiactis savignyi | Dodu |
Ophiopholis mirabilis | Gampo |
Class Echinoidea | |
Temnopleurus hardwickii | Mipo |
Phalacrocidaris japonica | Aewol |
Class Holothuroidea | |
Eupentacta chronhjelmi | Tongyeong |
Protankyra bidentata | Incheon |
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Kim, P.; Yoon, T.-J.; Shin, S. Monthly eDNA Monitoring of an Invasive Bryozoan, Bugulina californica, in Seawater Using Species-Specific Markers. Animals 2021, 11, 1966. https://doi.org/10.3390/ani11071966
Kim P, Yoon T-J, Shin S. Monthly eDNA Monitoring of an Invasive Bryozoan, Bugulina californica, in Seawater Using Species-Specific Markers. Animals. 2021; 11(7):1966. https://doi.org/10.3390/ani11071966
Chicago/Turabian StyleKim, Philjae, Tae-Joong Yoon, and Sook Shin. 2021. "Monthly eDNA Monitoring of an Invasive Bryozoan, Bugulina californica, in Seawater Using Species-Specific Markers" Animals 11, no. 7: 1966. https://doi.org/10.3390/ani11071966
APA StyleKim, P., Yoon, T.-J., & Shin, S. (2021). Monthly eDNA Monitoring of an Invasive Bryozoan, Bugulina californica, in Seawater Using Species-Specific Markers. Animals, 11(7), 1966. https://doi.org/10.3390/ani11071966