All Issue

2021 Vol.1, Issue 1 Preview Page

Original Articles

Metagenome Analysis of a Rhodolith Microbial Community Provides Evidence for Re-cycling of Nitrogen Sources within the Holobiont
JunMo Lee1
,
Hwan Su Yoon2*
1Department of Oceanography, Kyungpook National University, Daegu 41566, Korea
2Department of Biological Sciences, Sungkyunkwan University, Suwon 16419, Korea
*Corresponding Author
30 June 2021. pp. 57-69
PDF XML Citation
Abstract

Rhodoliths are calcareous nodules, composed of non-geniculate coralline red algae with tight association of diverse microbial eukaryotes, prokaryotes, and viruses. Rhodolith beds are generally distributed in coastal benthic environments and play crucial biogeochemical and ecological roles in marine benthic ecosystems. To better understand microbial interactions in rhodolith holobionts, we newly generated and analyzed metagenome sequencing data of a rhodolith. The presence of nitrogen cycling-related protein-coding genes from the strict anaerobic community (i.e., deltaproteobacteria) suggest that the rhodolith holobiont contains an anaerobic zone. In addition, we found both aerobic and anaerobic denitrification metabolisms that may play an important role for re-cycling of nitrogen metabolism within the holobiont. Therefore, it could be advantageous to the rhodolith holobiont to directly utilize recycled carbon and nitrogen. As a self-sustaining reservoir, rhodoltihs provide favorable habitats for diverse marine organisms.

Keywords
carbon cycling
coralline algae
holobiont
metagenome
nitrogen cycling
References
1
Adey WH and Macintyre IG. 1973. Crustose coralline algae: a re-evaluation in the geological sciences. Geol. Soc. Am. Bull. 84, 883-904. 10.1130/0016-7606(1973)84<883:CCAARI>2.0.CO;2
2
Adey W, Halfar J, Humphreys A, Suskiewicz T, Belanger D, Gagnon P and Fox M. 2015. Subarctic rhodolith beds promote longevity of crustose coralline algal buildups and their climate archiving potential. Palaios 30, 281-293. 10.2110/palo.2014.075
3
Aline T. 2008. Dissolution of dead corals by euendolithic microorganisms across the Northern Great Barrier Reef (Australia). Microb. Ecol. 55, 569-580. 10.1007/s00248-007-9302-617690835
4
Amado-Filho GM and Pereira-Filho GH. 2012. Rhodolith beds in Brazil: a new potential habitat for marine bioprospection. Rev. Bras. Farmacogn. 22, 782-788. 10.1590/S0102-695X2012005000066
5
Amado-Filho GM, Moura RL, Bastos AC, Salgado LT, Sumida PY, Guth AZ, Francini-Filho RB, Pereira-Filho GH, Abrantes DP, Brasileiro PS, Bahia RG, Leal RN, Kaufman L, Kleypas JA, Farina M and Thompson FL. 2012. Rhodolith beds are major CaCO3 bio-factories in the Tropical South West Atlantic. PLoS ONE 7, e35171. 10.1371/journal.pone.003517122536356PMC3335062
6
Amado-Filho GM, Bahia RG, Pereira-Filho GH and Longo LL. 2017. South Atlantic rhodolith beds: latitudinal distribution, species composition, structure and ecosystem functions, threats and conservation status. In: Rhodolith/maërl beds: a global perspective. Riosmena-Rodríguez R, Nelson W and Aguirre J, eds, Springer, Cham, 299-317. 10.1007/978-3-319-29315-8_12
7
Atkinson N, Feike D, Mackinder LCM, Meyer MT, Griffiths H, Jonikas MC, Smith AM and McCormick AJ. 2016. Introducing an algal carbon-concentrating mechanism into higher plants: location and incorporation of key components. Plant Biotechnol. J. 14, 1302-1315. 10.1111/pbi.1249726538195PMC5102585
8
Badger MR and Price GD. 1994. The role of carbonic anhydrase in photosynthesis. Annu. Rev. Plant Physiol. 45, 369-392. 10.1146/annurev.pp.45.060194.002101
9
Barott KL, Rodriguez-Brito B, Janouškovec J, Marhaver KL, Smith JE, Keeling P and Rohwer FL. 2011. Microbial diversity associated with four functional groups of benthic reef algae and the reef-building coral Montastraea annularis. Environ. Microbiol. 13, 1192-1204. 10.1111/j.1462-2920.2010.02419.x21272183
10
Basso D, Rodondi G and Bressan G. 2011. A re-description of Lithothamnion crispatum and the status of Lithothamnion superpositum (Rhodophyta, Corallinales). Phycologia 50, 144-155. 10.2216/10-20.1
11
Basso D. 2012. Carbonate production by calcareous red algae and global change. Geodiversitas 34, 13-34. 10.5252/g2012n1a2
12
Bertucci A, Moya A, Tambutté S, Allemand D, Supuran CT and Zoccola D. 2013. Carbonic anhydrases in anthozoan corals - a review. Bioorg. Med. Chem. 21, 1437-1450. 10.1016/j.bmc.2012.10.02423199478
13
Bianchi D, Weber TS, Kiko R and Deutsch C. 2018. Global niche of marine anaerobic metabolisms expanded by particle microenvironments. Nat. Geosci. 11, 263-268. 10.1038/s41561-018-0081-0
14
Birch PRJ, Rehmany AP, Pritchard L, Kamoun S and Beynon JL. 2006. Trafficking arms: oomycete effectors enter host plant cells. J. Mol. Evol. 14, 8-11. 10.1016/j.tim.2005.11.00716356717
15
Blouin NA, Brodie JA, Grossman AC, Xu P and Brawley SH. 2011. Porphyra: a marine crop shaped by stress. Trends Plant Sci. 16, 1360-1385. 10.1016/j.tplants.2010.10.00421067966
16
Bosence DWJ. 1983. Coralline algal reef frameworks. J. Geol. Soc. 140, 365-376. 10.1144/gsjgs.140.3.0365
17
Buchfink B, Xie C and Huson DH. 2015. Fast and sensitive protein alignment using DIAMOND. Nat. Methods 12, 59-60. 10.1038/nmeth.317625402007
18
Cabioch G, Montaggioni LF, Faure G and Ribaud-Lauernti A. 1999. Reef coralgal assemblages as recorders of paleobathymetry and sea level changes in the Indo-Pacific province. Quat. Sci. Rev. 18, 1681-1695. 10.1016/S0277-3791(99)00014-1
19
Capone DG and Carpenter EJ. 1982. Nitrogen fixation in the marine environment. Science 217, 1140-1142. 10.1126/science.217.4565.114017740970
20
Cavalcanti GS, Gregoracci GB, Longo LDL, Bastos AC, Ferreira CM, Francini-Filho RB, Parahos R, Ghisolfi RD, Krüger R, Güth AZ, Sumida PYG, Bruce T, Maia-Neto O, Santos EO, Iida T, Moura RL, Amado-Filho GM and Thompson FL. 2013. Sinkhole-like structures as bioproductivity hotspots in the Abrolhos Bank. Cont. Shelf Res. 70, 126-134. 10.1016/j.csr.2013.05.011
21
Cavalcanti GS, Gregoracci GB, Santos EOD, Silveira CB, Meirelles PM, Longo L, Gotoh K, Nakamura S, Iida T, Sawabe T, Rezende CE, Francini-Filho RB, Moura RL, Amado-Filho GM and Thompson FL. 2014. Physiologic and metagenomic attributes of the rhodoliths forming the largest CaCO3 bed in the South Atlantic Ocean. ISME J. 8, 52-62. 10.1038/ismej.2013.13323985749PMC3869012
22
Cavalcanti GS, Shukla P, Morris M, Ribeiro B, Foley M, Doane MP, Thompson CC, Edwards MS, Dinsdale EA and Thompson FL. 2018. Rhodoliths holobionts in a changing ocean: host-microbes interactions mediate coralline algae resilience under ocean acidification. BMC Genomics 19, 701. 10.1186/s12864-018-5064-430249182PMC6154897
23
Chan CX, Yang EC, Banerjee T, Yoon HS, Martone PT, Estevez JM and Bhattacharya D. 2011. Red and green algal monophyly and extensive gene sharing found in a rich repertoire of red algal genes. Curr. Biol. 21, 328-333. 10.1016/j.cub.2011.01.03721315598
24
Cheng Q. 2008. Perspectives in biological nitrogen fixation research. J. Integr. Plant Biol. 50, 786-798. 10.1111/j.1744-7909.2008.00700.x18713389
25
de Carvalho RT, Salgado LT, Amado-Filho GM, Leal RN, Werckmann J, Rossi AL, Campos APC, Karez CS and Farina M. 2017. Biomineralization of calcium carbonate in the cell wall of Lithothamnion crispatum (Hapalidiales, Rhodophyta): correlation between the organic matrix and the mineral phase. J. Phycol. 53, 642-651. 10.1111/jpy.1252628258584
26
de Oliveira LS, Gregoracci GB, Silva GGZ, Salgado LT, Amado-Filho G, Alves-Ferreira M, Pereira RC and Thompson FL. 2012. Transcriptomic analysis of the red seaweed Laurencia dendroidea (Florideophyceae, Rhodophyta) and its microbiome. BMC Genomics 13, 487. 10.1186/1471-2164-13-48722985125PMC3534612
27
Delmont TO, Quince C, Shaiber A, Esen ÖC, Lee ST, Rappé MS, McLellan SL, Lücker S and Eren AM. 2018. Nitrogen-fixing populations of Planctomycetes and Proteobacteria are abundant in surface ocean metagenomes. Nat. Microbiol. 3, 804-813. 10.1038/s41564-018-0176-929891866PMC6792437
28
Egan S, Harder T, Burke C, Steinberg P, Kjelleberg S and Thomas T. 2013. The seaweed holobiont: understanding seaweed-bacteria interactions. FEMS Microbiol. Rev. 37, 462-476. 10.1111/1574-6976.1201123157386
29
Fani R, Gallo R and Liò P. 2000. Molecular evolution of nitrogen fixation: the evolutionary history of the nifD, nifK, nifE, and nifN genes. J. Mol. Evol. 51, 1-11. 10.1007/s00239001006110903367
30
Farnelid H, Andersson AF, Bertilsson S, Al-Soud WA, Hansen LH, Sørensen S, Steward GF, Hagström Å and Riemann L. 2011. Nitrogenase gene amplicons from global marine surface waters are dominated by genes of non-cyanobacteria. PLoS One 6, e19223. 10.1371/journal.pone.001922321559425PMC3084785
31
Fredericq S, Krayesky-Self S, Sauvage T, Richards J, Kittle R, Arakaki N, Hickerson E and Schmidt WE. 2019. The critical importance of rhodoliths in the life cycle completion of both macro- and microalgae, and as holobionts for the establishment and maintenance of marine biodiversity. Front. Mar. Sci. 5, 502. 10.3389/fmars.2018.00502
32
Gabara SS. 2020. Trophic structure and potential carbon and nitrogen flow of a rhodolith bed at Santa Catalina Island inferred from stable isotopes. Mar. Biol. 167, 30. 10.1007/s00227-019-3635-9
33
Gao K, Aruga Y, Asada K, Ishihara T, Akano T and Kiyohara M. 1993. Calcification in the articulated coralline alga Corallina pilulifera, with special reference to the effect of elevated CO2 concentration. Mar. Biol. 117, 129-132. 10.1007/BF00346434
34
Gee CW and Niyogi KK. 2017. The carbonic anhydrase CAH1 is an essential component of the carbon-concentrating mechanism in Nannochloropsis oceanica. Proc. Natl. Acad. Sci. U.S.A. 114, 4537-4542. 10.1073/pnas.170013911428396394PMC5410810
35
Grall J, Loc'h FL, Guyonnet B and Riera P. 2006. Community structure and food web based on stable isotopes (δ15N and δ13C) analysis of a North Eastern Atlantic maerl bed. J. Exp. Mar. Biol. Ecol. 338, 1-15. 10.1016/j.jembe.2006.06.013
36
Grange JS, Rybarczyk H and Tribollet A. 2015. The three steps of the carbonate biogenic dissolution process by microborers in coral reefs (New Caledonia). Environ. Sci. Pollut. Res. 22, 13625-13637. 10.1007/s11356-014-4069-z25592911
37
Greene AC. 2014. The Family Desulfuromonadaceae. In: The Prokaryotes Deltaproteobacteria and Epsilonproteobacteria. Rosenberg E, DeLong EF, Lory S, Stackebrandt E and Thompson F, eds, Springer-Verlag, Berlin Heidelberg, 143-155.
38
Halfar J, Zack T, Kronz A and Zachos JC. 2000. Growth and high-resolution paleoenvironmental signals of rhodoliths (coralline red algae): a new biogenic archive. J. Geophys. Res. 105, 22107-22116. 10.1029/1999JC000128
39
Harris PT, Tsuji Y, Marshall JF, Davies PJ, Honda N and Matsuda H. 1996. Sand ans rhodolith-gravel entrainment on the mid- to outer-shelf under a western boundary current: Fraser Island continental shelf, eastern Australia. Mar. Geol. 129, 313-330. 10.1016/0025-3227(96)83350-0
40
Horta PA, Riul P, Amado-Filho GM, Gurgel CFD, Berchez F, Nunes JMDC, Scherner F, Pereira S, Lotufo T, Peres L, Sissini M, Bastos EO, Rosa J, Munoz P, Martins C, Gouvêa L, Carvalho V, Bergstrom E, Schubert N, Bahia RG, Rodrigues AC, Rörig L, Barufi JB and Figueiredo M. 2016. Rhodoliths in Brazil: current knowledge and potential impacts of climate change. Braz. J. Oceanogr. 64, 117-136. 10.1590/S1679-875920160870064sp2
41
Huppe HC and Turpin DH. 1994. Integration of carbon and nitrogen metabolism in plan and algal cells. Annu. Rev. Plant Biol. 45, 577-607. 10.1146/annurev.pp.45.060194.003045
42
Hwang EK, Gong YG and Park CS. 2010. Ecological characteristics of the endangered brown alga, Undariopsis peterseniana (Kjellman) Miyabe et Okamura, at Jeju Island, Korea: growth and maturation. Korean J. Fish. Aquat. Sci. 43, 63-68. 10.5657/kfas.2010.43.1.063
43
Hyatt D, Chen GL, LoCascio PF, Land ML, Larimer FW and Hauser LJ. 2010. Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC Bionfiormatics 11, 119. 10.1186/1471-2105-11-11920211023PMC2848648
44
Janouškovec J, Horák A, Barott KL, Rohwer FL and Keeling PJ. 2012. Global analysis of platid diversity reveals apicomplexan-related lineages in coral reefs. Curr. Biol. 22, R518-R519. 10.1016/j.cub.2012.04.04722789997
45
Janouškovec J, Horák A, Barott KL, Rohwer FL and Keeling PJ. 2013. Environmental distribution of coral-associated relatives of apicomplexan parasites. ISME J. 7, 444-447. 10.1038/ismej.2012.12923151646PMC3554414
46
Jeong JB, Kim SY, Seo YK, Kim JK, Shin J and Woo KS. 2020. Influence of submarine topography and associated sedimentary processes on the distribution of live and dead rhodoliths near Udo Island, Korea. Geo-Mar. Lett. 40, 35-51. 10.1007/s00367-019-00623-w
47
Kamenos NA and Law A. 2010. Temperature controls on coralline algal skeletal growth. J. Phycol. 46, 331-335. 10.1111/j.1529-8817.2009.00780.x
48
Kim JH, Steller DL and Edwards MS. 2021. Variation in photosynthetic performance relative to thallus microhabitat heterogeneity in Lithothamnion australe (Rhodophyta, Corallinales) rhodoliths. J. Phycol. 57, 234-244. 10.1111/jpy.1308033020935
49
Koh YH and Kim MS. 2018. DNA barcoding reveals cryptic diversity of economic red algae, Pyropia (Bangiales, Rhodophyta): description of novel species from Korea. J. Appl. Phycol. 30, 3425-3434. 10.1007/s10811-018-1529-8
50
Krayesky-Self S, Schmidt WE, Phung D, Henry C, Sauvage T, Camacho O, Felgenhauer BE, Fredericq S. 2017. Eukaryotic life inhabits rhodolith-forming coralline algae (Haplidiales, Rhodophyta), remarkable marine benthic microhabitats. Sci. Rep. 7, 45850. 10.1038/srep4585028368049PMC5377461
51
Kucera H and Saunders GW. 2012. A survey of Bangiales (Rhodophyta) based on multiple molecular markers reveals cryptic diversity. J. Phycol. 48, 869-882. 10.1111/j.1529-8817.2012.01193.x27008998
52
Kuever J. 2014a. The Family Desulfobacteraceae. In: The Prokaryotes Deltaproteobacteria and Epsilonproteobacteria. Rosenberg E, DeLong EF, Lory S, Stackebrandt E and Thompson F, eds, Springer-Verlag, Berlin Heidelberg, 45-73.
53
Kuever J. 2014b. The Family Desulfobulbaceae. In: The Prokaryotes Deltaproteobacteria and Epsilonproteobacteria. Rosenberg E, DeLong EF, Lory S, Stackebrandt E and Thompson F, eds, Springer-Verlag, Berlin Heidelberg, 75-86.
54
Lagesen K, Hallin P, Rødland EA, Staerfeldt H, Rognes T and Ussery DW. 2007. RNAmmer: consistent and rapid annotation of ribosomal RNA genes. Nucleic Acids Res. 35, 3100-3108. 10.1093/nar/gkm16017452365PMC1888812
55
Lee JM, Song HJ, Park SI, Lee YM, Jeong SY, Cho TO, Kim JH, Choi HG, Choi CG, Nelson WA, Fredericq S, Bhattacharya D and Yoon HS. 2018. Mitochondrial and plastid genomes from coralline red algae provide insights into the incongruent evolutionary histories of organelles. Genome Biol. Evol. 10, 2961-2972. 10.1093/gbe/evy22230364957PMC6279150
56
Lennon JT and Jones SE. 2011. Microbial seed banks: the ecological and evolutionary implications of dormancy. Nat. Rev. Microbiol. 9, 119-130. 10.1038/nrmicro250421233850
57
Li D, Liu C, Luo R, Sadakane K and Lam T. 2015. MEGAHIT: an ultra-fast single-node solution for large and complex metagenomics assembly via succinct de Bruijn graph. Bioinformatics 31, 1674-1676. 10.1093/bioinformatics/btv03325609793
58
Macler BA. 1986. Regulation of carbon flow by nitrogen and light in the red alga, Gelidium coulteri. Plant Physiol. 82, 136-141. 10.1104/pp.82.1.13616664980PMC1056079
59
Marcelino VR and Verbruggen H. 2016. Multi-marker metabarcoding of coral skeletons reveals a rich microbiome and diverse evolutionary origins of endolithic algae. Sci. Rep. 6, 31508. 10.1038/srep3150827545322PMC4992875
60
Massé A, Domart-Coulon I, Golubic S, Duché D and Tribollet A. 2018. Early skeletal colonization of the coral holobiont by the microboring Ulvophyceae Ostreobium sp.. Sci. Rep. 8, 2293. 10.1038/s41598-018-20196-529396559PMC5797222
61
Matson EA and Quenga ASE. 2005. A nitrogen budget, including the occurrence and activity of nitrogen fixers in nitrogen-rich and nitrogen-poor habitats of Guam, Mariana Islands. Micronesica 37, 271-285.
62
McCoy SJ and Kamenos NA. 2015. Coraline algae (Rhodophyta) in a changing world: integrating ecological, physiological, and geochemical responses to global change. J. Phycol. 51, 6-24. 10.1111/jpy.1226226986255PMC4964943
63
Nguyen LT, Schmidt HA, Von Haeseler A and Minh BQ. 2015. IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol. Biol. Evol. 32, 268-274. 10.1093/molbev/msu30025371430PMC4271533
64
Pais M, Win J, Yoshida K, Etherington GJ, Cano LM, Raffaele S, Banfield MJ, Jones A, Kamoun S and Saunders DGO. 2013. From pathogen genomes to host plant processes: the power of plant parasitic oomycetes. Genome Biol. 14, 211. 10.1186/gb-2013-14-6-21123809564PMC3706818
65
Phlips EJ and Zeman C. 1990. Photosynthesis, growth and nitrogen fixation by epiphytic forms of filamentous cyanobacteria from pelagic Sargassum. Bull. Mar. Sci. 47, 613-621.
66
Razzak MA, Lee JM, Lee DW, Kim JH, Yoon HS and Hwang I. 2019. Expression of seven carbonic anhydrases in red alga Gracilariopsis chorda and their subcellular localization in a heterologous system, Arabidopsis thaliana. Plant Cell Rep. 38, 147-159. 10.1007/s00299-018-2356-830446790
67
Richards TA, Soanes DM, Jones MDM, Vasieva O, Leonard G, Paszkiewicz K, Foster PG, Hall N and Talbot NJ. 2011. Horizontal gene transfer facilitated the evolution of plant parasitic mechanisms in the oomycetes. Proc. Natl. Acad. Sci. U.S.A. 108, 15258-15263. 10.1073/pnas.110510010821878562PMC3174590
68
Riemann L, Farnelid H and Steward GF. 2010. Nitrogenase genes in non-cyanobacterial plankton: prevalence, diversity and regulation in marine waters. Aquat. Microb. Ecol. 61, 235-247. 10.3354/ame01431
69
Schubert N, Salazar VW, Rich WA, Bercovich MV, Saá ACA, Fadigas SD, Silva J and Horta PA. 2019. Rhodolith primary and carbonate production in a changing ocean: the interplay of warming and nutrients. Sci. Total Environ. 676, 455-468. 10.1016/j.scitotenv.2019.04.28031048175
70
Sohm JA, Webb EA and Capone DG. 2011. Emerging patterns of marine nitrogen fixation. Nat. Rev. Microbiol. 9, 499-508. 10.1038/nrmicro259421677685
71
Supuran CT and Capasso C. 2017. An overview of the bacterial carbonic anhydrases. Metabolites 7, 56. 10.3390/metabo704005629137134PMC5746736
72
Tamames J and Puente-Sánchez F. 2019. SqueezeMeta, a highly portable, fully automatic metagenomic analysis pipeline. Front. Microbiol. 9, 3349. 10.3389/fmicb.2018.0334930733714PMC6353838
73
Teed L, Bélanger D, Gagnon P and Edinger E. 2020. Calcium carbonate (CaCO3) production of a subpolar rhodolith bed: methods of estimation, effect of bioturbators, and global comparisons. Estuar. Coast. Shelf Sci. 242, 106822. 10.1016/j.ecss.2020.106822
74
Testa V and Bosence DWJ. 1999. Physical and biological controls on the formation of carbonate and siliciclastic bedforms on the north‐east Brazilian shelf. Sedimentology 46, 279-301. 10.1046/j.1365-3091.1999.00213.x
75
Thines M and Kamoun S. 2010. Oomycete-plant coevolution: recent advances and future prospects. Curr. Plant Biol. 13, 427-433. 10.1016/j.pbi.2010.04.00120447858
76
Zhou W, Sui Z, Wang J, Hu Y, Kang KH, Hong HR, Niaz Z, Wei H, Du Q, Peng C, Mi P and Que Z. 2016. Effects of sodium bicarbonate concentration on growth, photosynthesis, and carbonic anhydrase activity of macroalgae Gracilariopsis lemaneiformis, Gracilaria vermiculophylla, and Gracilaria chouae (Gracilariales, Rhodophyta). Photosynth. Res. 128, 259-270. 10.1007/s11120-016-0240-326960545
77
van der Loos LM, Eriksson BK and Salles JF. 2019. The macroalgal holobiont in a changing sea. Trends Microbiol. 27, 635-650. 10.1016/j.tim.2019.03.00231056303
78
Verbruggen H, Marcelino VR, Guiry MD, Cremen MCM and Jackson CJ. 2017. Phylogenetic position of the coral symbiont Ostreobium (Ulvophyceae) inferred from chloroplast genome data. J. Phycol. 53, 790-803. 10.1111/jpy.1254028394415
79
Wang D, Yu X, Xu K, Bi G, Cao M, Zelzion E, Fu C, Sun P, Liu Y, Kong F, Du G, Tang X, Yang R, Wang J, Tang L, Wang L, Zhao Y, Ge Y, Zhuang Y, Mo Z, Chen Y, Gao T, Huan X, Chen R, Qu W, Sun B, Bhattachary D and Mao Y. 2020. Pyropia yezoensis genome reveals diverse mechanisms of carbon acquisition in the intertidal environment. Nat. Commun. 11, 4028. 10.1038/s41467-020-17689-132788591PMC7423979
80
Williams B, Halfar J, Steneck RS, Wortmann UG, Hetzinger S, Adey W, Lebednik P and Joachimski M. 2011. Twentieth century δ13C variability in surface water dissolved inorganic carbon recorded by coralline algae in the northern North Pacific Ocean and the Bering Sea. Biogeosciences 8, 165-174. 10.5194/bg-8-165-2011
81
Yamada KD, Tomii K and Katoh K. 2016. Application of the MAFFT sequence alignment program to large data-reexamination of the usefulness of chained guide trees. Bioinformatics 32, 3246-3251. 10.1093/bioinformatics/btw41227378296PMC5079479
82
Zehr JP and Capone DG. 2020. Changing perspectives in marine nitrogen fixation. Science 368, eaay9514. 10.1126/science.aay951432409447
83
Zhang X, Ward BB and Sigman DM. 2020. Global nitrogen cycle: critical enzymes, organisms, and processes for nitrogen budgets and dynamics. Chem. Rev. 120, 5308-5351. 10.1021/acs.chemrev.9b0061332530264
Information
  • Publisher :The Korean Society of Phycology
  • Publisher(Ko) :한국조류학회
  • Journal Title :Aquatic Nature
  • Journal Title(Ko) :수생생물
  • Volume : 1
  • No :1
  • Pages :57-69
  • Received Date : 2021-05-26
  • Revised Date : 2021-06-16
  • Accepted Date : 2021-06-22
  • DOI :https://doi.org/10.23135/an.2021.1.1.6
Journal Informaiton Aquatic Nature Aquatic Nature
Online Submission
  • KISTI Current Status
  • KISTI Cited-by
  • open access
  • ccl
Journal Informaiton Journal Informaiton - close