

FOLLOWUS
Key Laboratory of Marine Genetics and Breeding (Ministry of Education), College of Marine Life Sciences, Ocean University of China, Qingdao 266003, China
txianghai@ouc.edu.cn
Received:30 April 2023,
Online First:30 June 2023,
Published:01 November 2023
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WANG Xinran,WANG Junhao,ZHU Yunke,et al.Comparison in structure and predicted function of epiphytic bacteria on Neopyropia yezoensis and Neopyropia katadae[J].Journal of Oceanology and Limnology,2023,41(06):2232-2248.
The economic alga
Neopyropia
which holds significant value in China for its edibility and economic potential
harbors diverse epiphytic bacteria on its surface. The epiphytic bacteria on
Neopyropia yezoensis
and
Neopyropia katadae
two nori species of
Neopyropia
living at the same tidal level but with distinct physiological states and living habits
were investigated to understand the differences between them and the effects of epiphytic bacteria on their differential characteristics. Analysis of 16S rRNA gene sequences and real-time quantitative PCR (qPCR) of thalli and seawater samples (
n
=24) revealed notable differences in microbial diversity and community structure between the two species. Bacteroidetes
dominated the bacterial communities in association with
N
.
yezoensis
whereas Proteobacteria were predominant in
N
.
katadae
. Phylogenetic Investigation of Communities by Reconstruction of Unobserved States (PICRUSt2) analysis revealed enriched genes that related to the ABC transport system
iron complex outer membrane receptor proteins
and proliferation in
N
.
yezoensis
whereas
N
.
katadae
exhibited enrichment of genes that related to energy supply as well as cell wall and cell membrane production.The results of qPCR indicate a higher abundance of epiphytic bacteria on surface of
N
.
yezoensis
than those on surface of
N
.
katadae
. The findings indicate that differences in the living environments of
N
.
yezoensis
and
N
.
katadae
may result in distinct structural composition and abundance of epiphyt
ic bacteria on their surfaces
thereby conferring specific biological functionalities to each microbial community
and the epiphytic bacteria may shape the living habits of hosts to some extents. This study provided a basis for understanding the close association between surface microorganisms and algal bodies
and the physiological and ecological characteristics of nori species.
Ahmed A , Khurshid A , Tang X H et al . 2021 . Structural and functional impacts of microbiota on Pyropia yezoensis and surrounding seawater in cultivation farms along coastal areas of the Yellow Sea . Microorganisms , 9 ( 6 ): 1291 , https://doi.org/10.3390/microorganisms9061291 https://doi.org/10.3390/microorganisms9061291 .
Alonso C , Warnecke F , Amann R et al . 2007 . High local and global diversity of Flavobacteria in marine plankton . Environmental Microbiology , 9 ( 5 ): 1253 - 1266 , https://doi.org/10.1111/j.1462-2920.2007.01244.x https://doi.org/10.1111/j.1462-2920.2007.01244.x .
Anraku Y , Gennis R B . 1987 . The aerobic respiratory chain of Escherichia coli . Trends in Biochemical Sciences , 12 : 262 - 266 , https://doi.org/10.1016/0968-0004(87)90131-9 https://doi.org/10.1016/0968-0004(87)90131-9 .
Bathnagar D , Deb A R . 1978 . Some effects of pregermination exposure of wheat seeds to magnetic field. II. Effect on some physiological processes . Seed Research , 6 ( 1 ): 14 - 22 .
Benhamou N , Thériault G . 1992 . Treatment with chitosan enhances resistance of tomato plants to the crown and root rot pathogen Fusarium oxysporum f. sp. radicis - lycopersici . Physiological and Molecular Plant Pathology , 41 ( 1 ): 33 - 52 , https://doi.org/10.1016/0885-5765(92)90047-Y https://doi.org/10.1016/0885-5765(92)90047-Y .
Bernardet J F , Segers P , Vancanneyt M et al . 1996 . Cutting a Gordian knot: emended classification and description of the genus Flavobacterium , emended description of the family Flavobacteriaceae, and proposal of Flavobacterium hydatis nom. nov . (Basonym, Cytophaga aquatilis Strohl and Tait 1978 ). International Journal of Systematic Bacteriology, 46 ( 1 ): 128 - 148 , https://doi.org/10.1099/00207713-46-1-128 https://doi.org/10.1099/00207713-46-1-128 .
Bi H K , Wang H H , Cronan J E . 2013 . FabQ, a dual-function dehydratase/isomerase, circumvents the last step of the classical fatty acid synthesis cycle . Chemistry & Biology , 20 ( 9 ): 1157 - 1167 , https://doi.org/10.1016/j.chembiol.2013.07.007 https://doi.org/10.1016/j.chembiol.2013.07.007 .
Biegala I C , Kennaway G , Alverca E et al . 2002 . Identification of bacteria associated with Dinoflagellates (Dinophyceae) Alexandrium spp. using tyramide signal amplification-fluorescent in situ hybridization and confocal microscopy . Journal of Phycology , 38 ( 2 ): 404 - 411 , https://doi.org/10.1046/j.1529-8817.2002.01045.x https://doi.org/10.1046/j.1529-8817.2002.01045.x .
Bolyen E , Rideout J R , Dillon M R et al . 2019 . Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2 . Nature Biotechnology , 37 ( 8 ): 852 - 857 , https://doi.org/10.1038/s41587-019-0209-9 https://doi.org/10.1038/s41587-019-0209-9 .
Bulleri F , Chapman M G . 2010 . The introduction of coastal infrastructure as a driver of change in marine environments . Journal of Applied Ecology , 47 ( 1 ): 26 - 35 , https://doi.org/10.1111/j.1365-2664.2009.01751.x https://doi.org/10.1111/j.1365-2664.2009.01751.x .
Callahan B J , McMurdie P J , Rosen M J et al . 2016 . DADA2: high-resolution sample inference from Illumina amplicon data . Nature Methods , 13 ( 7 ): 581 - 583 , https://doi.org/10.1038/nmeth.3869 https://doi.org/10.1038/nmeth.3869 .
Campbell A H , Marzinelli E M , Gelber J et al . 2015 . Spatial variability of microbial assemblages associated with a dominant habitat-forming seaweed . Frontiers in Microbiology , 6 : 230 , https://doi.org/10.3389/fmicb.2015.00230 https://doi.org/10.3389/fmicb.2015.00230 .
Chapman M G , Underwood A J . 1999 . Ecological patterns in multivariate assemblages: information and interpretation of negative values in ANOSIM tests . Marine Ecology Progress Series , 180 : 257 - 265 , https://doi.org/10.3354/meps180257 https://doi.org/10.3354/meps180257 .
Chen Z J , Shao Y , Li Y J et al . 2020 . Rhizosphere bacterial community structure and predicted functional analysis in the water-level fluctuation zone of the Danjiangkou Reservoir in China during the dry period . International Journal of Environmental Research and Public Health , 17 ( 4 ): 1266 , https://doi.org/10.3390/ijerph17041266 https://doi.org/10.3390/ijerph17041266 .
Cook K , Vanderklift M A , Poore A G B . 2011 . Strong effects of herbivorous amphipods on epiphyte biomass in a temperate seagrass meadow . Marine Ecology Progress Series , 442 : 263 - 269 , https://doi.org/10.3354/meps09446 https://doi.org/10.3354/meps09446 .
Cosgrove D J . 2005 . Growth of the plant cell wall . Nature Reviews Molecular Cell Biology , 6 ( 11 ): 850 - 861 , https://doi.org/10.1038/nrm1746 https://doi.org/10.1038/nrm1746 .
Cottrell M T , Kirchman D L . 2000a . Community composition of marine bacterioplankton determined by 16S rRNA gene clone libraries and fluorescence in situ hybridization . Applied and Environmental Microbiology , 66 ( 12 ): 5116 - 5122 , https://doi.org/10.1128/AEM.66.12.5116-5122.2000 https://doi.org/10.1128/AEM.66.12.5116-5122.2000 .
Cottrell M T , Kirchman D L . 2000b . Natural assemblages of marine proteobacteria and member s of the Cytophaga - Flavobacter cluster consuming low- and high-molecular-weight dissolved organic matter . Applied and Environmental Microbiology , 66 ( 4 ): 1692 - 1697 , https://doi.org/10.1128/AEM.66.4.1692-1697.2000 https://doi.org/10.1128/AEM.66.4.1692-1697.2000 .
Croft M T , Lawrence A D , Raux-Deery E et al . 2005 . Algae acquire vitamin B 12 through a symbiotic relationship with bacteria . Nature , 438 ( 7064 ): 90 - 93 , https://doi.org/10.1038/nature04056 https://doi.org/10.1038/nature04056 .
Croft M T , Warren M J , Smith A G . 2006 . Algae need their vitamins . Eukaryotic Cell , 5 ( 8 ): 1175 - 1183 . https://doi.org/10.1128/EC.00097-06 https://doi.org/10.1128/EC.00097-06 .
Cruz-López R , Maske H . 2016 . The vitamin B 1 and B 12 required by the marine dinoflagellate Lingulodinium polyedrum can be provided by its associated bacterial community in culture. Frontiers in Microbiology , 7 : 560 , https://doi.org/10.3389/fmicb.2016.00560 https://doi.org/10.3389/fmicb.2016.00560 .
Davidson A L , Chen J . 2004 . ATP-binding cassette transporters in bacteria . Annual Review of Biochemistry , 73 ( 1 ): 241 , https://doi.org/10.1146/annurev.biochem.73.011303.073626 https://doi.org/10.1146/annurev.biochem.73.011303.073626 .
Davison I R , Pearson G A . 1996 . Stress tolerance in intertidal seaweeds . Journal of Phycology , 32 ( 2 ): 197 - 211 , https://doi.org/10.1111/j.0022-3646.1996.00197.x https://doi.org/10.1111/j.0022-3646.1996.00197.x .
Delattre C , Fenoradosoa T A , Michaud P . 2011 . Galactans: an overview of their most important sourcing and applications as natural polysaccharides . Brazilian Archives of Biology and Technology , 54 ( 6 ): 1075 - 1092 , https://doi.org/10.1590/S1516-89132011000600002 https://doi.org/10.1590/S1516-89132011000600002 .
Douglas G M , Maffei V J , Zaneveld J et al . 2019 . PICRUSt2: an improved and extensible approach for metagenome inference . BioRxiv , https://doi.org/10.1101/672295 https://doi.org/10.1101/672295 .
Egan S , Thomas T . 2015 . Editorial for: microbial symbiosis of marine sessile hosts-diversity and function . Frontiers in Microbiology , 6 : 585 , https://doi.org/10.3389/fmicb.2015.00585 https://doi.org/10.3389/fmicb.2015.00585 .
Falkowski P G , Katz M E , Knoll A H et al . 2004 . The evolution of modern eukaryotic phytoplankton . Science , 305 ( 5682 ): 354 - 360 , https://doi.org/10.1126/science.1095964 https://doi.org/10.1126/science.1095964 .
Gao M , Xiong C , Gao C et al . 2021 . Disease-induced changes in plant microbiome assembly and functional adaptation . Microbiome , 9 ( 1 ): 187 , https://doi.org/10.1186/s40168-021-01138-2 https://doi.org/10.1186/s40168-021-01138-2 .
Giraud M F , Naismith J H . 2000 . The rhamnose pathway . Current Opinion in Structural Biology , 10 ( 6 ): 687 - 696 , https://doi.org/10.1016/S0959-440X(00)00145-7 https://doi.org/10.1016/S0959-440X(00)00145-7 .
Goecke F , Labes A , Wiese J et al . 2010 . Chemical interactions between marine macroalgae and bacteria . Marine Ecology Progress Series , 409 : 267 - 299 , https://doi.org/10.3354/meps08607 https://doi.org/10.3354/meps08607 .
Haas B J , Gevers D , Earl A M et al . 2011 . Chimeric 16S rRNA sequence formation and detection in Sanger and 454-pyrosequenced PCR amplicons . Genome Research , 21 ( 3 ): 494 - 504 , https://doi.org/10.1101/gr.112730.110 https://doi.org/10.1101/gr.112730.110 .
Hartman W H , Ye R Z , Horwath W R et al . 2017 . A genomic perspective on stoichiometric regulation of soil carbon cycling . The ISME Journal , 11 ( 12 ): 2652 - 2665 , https://doi.org/10.1038/ismej.2017.115 https://doi.org/10.1038/ismej.2017.115 .
Helliwell K E , Wheeler G L , Leptos K C et al . 2011 . Insights into the evolution of vitamin B 12 auxotrophy from sequenced algal genomes . Molecular Biology and Evolution , 28 ( 10 ): 2921 - 2933 , https://doi.org/10.1093/molbev/msr124 https://doi.org/10.1093/molbev/msr124 .
Hollenstein K , Dawson R J , Locher K P . 2007 . Structure and mechanism of ABC transporter proteins . Current Opinion in Structural Biology , 17 ( 4 ): 412 - 418 , https://doi.org/10.1016/j.sbi.2007.07.003 https://doi.org/10.1016/j.sbi.2007.07.003 .
Jalilian N , Najafpour G D , Khajouei M . 2019 . Enhanced vitamin B 12 production using Chlorella vulgaris . International Journal of Engineering , 32 ( 1 ): 1 - 9 , https://doi.org/10.5829/ije.2019.32.01a.01 https://doi.org/10.5829/ije.2019.32.01a.01 .
Ji Y , Xu Z G , Zou D H et al . 2016 . Ecophysiological responses of marine macroalgae to climate change factors . Journal of Applied Phycology , 28 ( 5 ): 2953 - 2967 , https://doi.org/10.1007/s10811-016-0840-5 https://doi.org/10.1007/s10811-016-0840-5 .
Johansen J E , Nielsen P , Sjøholm C . 1999 . Description of Cellulophaga baltica gen. nov., sp. nov. and Cellulophaga fucicola gen. nov., sp. nov. and reclassification of [ Cytophaga ] lytica to Cellulophaga lytica gen. nov., comb. nov . International Journal of Systematic and Evolutionary Microbiology , 49 ( 3 ): 1231 - 1240 , https://doi.org/10.1099/00207713-49-3-1231 https://doi.org/10.1099/00207713-49-3-1231 .
Kendra D F , Hadwiger L A . 1984 . Characterization of the smallest chitosan oligomer that is maximally antifungal to Fusarium solani and elicits pisatin formation in Pisum sativum . Experimental Mycology , 8 ( 3 ): 276 - 281 , https://doi.org/10.1016/0147-5975(84)90013-6 https://doi.org/10.1016/0147-5975(84)90013-6 .
Keshtacher-Liebso E , Hadar Y , Chen Y . 1995 . Oligotrophic bacteria enhance algal growth under iron-deficient conditions . Applied and Environmental Microbiology , 61 ( 6 ): 2439 - 2441 , https://doi.org/10.1128/aem.61.6.2439-2441.1995 https://doi.org/10.1128/aem.61.6.2439-2441.1995 .
Kuznetsova E , Proudfoot M , Gonzalez C F et al . 2006 . Genome-wide analysis of substrate specificities of the Escherichia coli haloacid dehalogenase-like phosphatase family . Journal of Biological Chemistry , 281 ( 47 ): 36149 - 36161 , https://doi.org/10.1074/jbc.M605449200 https://doi.org/10.1074/jbc.M605449200 .
Lam E , Kato N , Lawton M . 2001 . Programmed cell death, mitochondria and the plant hypersensitive response . Nature , 411 ( 6839 ): 848 - 853 , https://doi.org/10.1038/35081184 https://doi.org/10.1038/35081184 .
Langille M G I , Zaneveld J , Caporaso J G et al . 2013 . Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences . Nature Biotechnology , 31 ( 9 ): 814 - 821 , https://doi.org/10.1038/nbt.267 https://doi.org/10.1038/nbt.267 .
Lebrun E S , Kang S . 2018 . A comparison of computationally predicted functional metagenomes and microarray analysis for microbial P cycle genes in a unique basalt-soil forest . F1000Research , 7 : 179 , https://doi.org/10.12688/f1000research.13841.1 https://doi.org/10.12688/f1000research.13841.1 .
Lennon A M , Neuenschwander U H , Ribas-Carbo M et al . 1997 . The effects of salicylic acid and tobacco mosaic virus infection on the alternative oxidase of tobacco . Plant Physiology , 115 ( 2 ): 783 - 791 , https://doi.org/10.1104/pp.115.2.783 https://doi.org/10.1104/pp.115.2.783 .
Li B , Zhang X X , Guo F et al . 2013 . Characterization of tetracycline resistant bacterial community in saline activated sludge using batch stress incubation with high-throughput sequencing analysis . Water Research , 47 ( 13 ): 4207 - 4216 , https://doi.org/10.1016/j.watres.2013.04.021 https://doi.org/10.1016/j.watres.2013.04.021 .
Li T D , Doronina N V , Ivanova E G et al . 2007 . Vitamin B 12 -independent strains of Methylophaga marina isolated from Red Sea algae . Microbiology , 76 ( 1 ): 75 - 81 , https://doi.org/10.1134/S0026261707010110 https://doi.org/10.1134/S0026261707010110 .
Lin A P , Wang G C , Yang F et al . 2009 . Photosynthetic parameters of sexually different parts of Porphyra katadai var. hemiphylla (Bangiales, Rhodophyta) during dehydration and re-hydration . Planta , 229 ( 4 ): 803 - 810 , https://doi.org/10.1007/s00425-008-0874-2 https://doi.org/10.1007/s00425-008-0874-2 .
Lux R , Jahreis K , Bettenbrock K et al . 1995 . Coupling the phosphotransferase system and the methyl-accepting chemotaxis protein-dependent chemotaxis signaling pathways of Escherichia coli . Proceedings of the National Academy of Sciences of the United States of America , 92 ( 25 ): 11583 - 11587 , https://doi.org/10.1073/pnas.92.25.11583 https://doi.org/10.1073/pnas.92.25.11583 .
Lyngstadaas A , Løbner-Olesen A , Boye E . 1995 . Characterization of three genes in the dam-containing operon of Escherichia coli . Molecular and General Genetics MGG , 247 ( 5 ): 546 - 554 , https://doi.org/10.1007/BF00290345 https://doi.org/10.1007/BF00290345 .
Lyngstadaas A , Løbner-Olesen A , Grelland E et al . 1999 . The gene for 2-phosphoglycolate phosphatase ( gph ) in Escherichia coli is located in the same operon as dam and at least five other diverse genes . Biochimica et Biophysica Acta (BBA)-General Subjects , 1472 ( 1-2 ): 376 - 384 , https://doi.org/10.1016/S0304-4165(99)00146-4 https://doi.org/10.1016/S0304-4165(99)00146-4 .
Magoč T , Salzberg S L . 2011 . FLASH: fast length adjustment of short reads to improve genome assemblies . Bioinformatics , 27 ( 21 ): 2957 - 2963 , https://doi.org/10.1093/bioinformatics/btr507 https://doi.org/10.1093/bioinformatics/btr507 .
Manz W , Amann R , Ludwig W et al . 1996 . Application of a suite of 16S rRNA-specific oligonucleotide probes designed to investigate bacteria of the phylum cytophaga-flavobacter-bacteroides in the natural environment . Microbiology , 142 ( 5 ): 1097 - 1106 , https://doi.org/10.1099/13500872-142-5-1097 https://doi.org/10.1099/13500872-142-5-1097 .
Marinković B , Grujić M , Marinković D et al . 2008 . Use of biophysical methods to improve yields and quality of agricultural products . Journal of Agricultural Sciences, Belgrade , 53 ( 3 ): 235 - 242 , https://doi.org/10.2298/JAS0803235M https://doi.org/10.2298/JAS0803235M .
Mercado J , Niell F X . 2000 . Carbon dioxide uptake by Bostrychia scorpioides (Rhodophyceae) under emersed conditions . British Phycological Bulletin , 35 ( 1 ): 45 - 51 , https://doi.org/10.1080/09670260010001735611 https://doi.org/10.1080/09670260010001735611 .
Nakayama Y , Hayashi M , Yoshikawa K et al . 1999 . Inhibitor studies of a new antibiotic, korormicin, 2-n-heptyl-4-hydroxyquinoline N -oxide and Ag + toward the Na + -translocating NADH-quinone reductase from the marine Vibrio alginolyticus . Biological and Pharmaceutical Bulletin , 22 ( 10 ): 1064 - 1067 , https://doi.org/10.1248/bpb.22.1064 https://doi.org/10.1248/bpb.22.1064 .
Nichols C M , Bowman J P , Guezennec J . 2005 . Olleya marilimosa gen. nov., sp. nov., an exopolysaccharide-producing marine bacterium from the family Flavobacteriaceae , isolated from the Southern Ocean . International Journal of Systematic and Evolutionary Microbiology , 55 ( 4 ): 1557 - 1561 , https://doi.org/10.1099/ijs.0.63642-0 https://doi.org/10.1099/ijs.0.63642-0 .
Pellicer M T , Nuñez M F , Aguilar J et al . 2003 . Role of 2-phosphoglycolate phosphatase of Escherichia coli in metabolism of the 2-phosphoglycolate formed in DNA repair . Journal of Bacteriology , 185 ( 19 ): 5815 - 5821 , https://doi.org/10.1128/JB.185.19.5815-5821.2003 https://doi.org/10.1128/JB.185.19.5815-5821.2003 .
Pospieszny H , Chirkov S , Atabekov J . 1991 . Induction of antiviral resistance in plants by chitosan . Plant Science , 79 ( 1 ): 63 - 68 , https://doi.org/10.1016/0168-9452(91)90070-O https://doi.org/10.1016/0168-9452(91)90070-O .
Provasoli L , Carlucci A . 1974 . Vitamins and growth regulators . In: Stewart W D P ed . Algal Physiology and Biochemistry, Botanical Monographs. University of California Press, Berkeley. p. 741 - 787 .
Ribeiro H , de Sousa T , Santos J P et al . 2018 . Potential of dissimilatory nitrate reduction pathways in polycyclic aromatic hydrocarbon degradation . Chemosphere , 199 : 54 - 67 , https://doi.org/10.1016/j.chemosphere.2018.01.171 https://doi.org/10.1016/j.chemosphere.2018.01.171 .
Rusch D B , Halpern A L , Sutton G et al . 2007 . The Sorcerer II global ocean sampling expedition: northwest Atlantic through eastern tropical Pacific . PLoS Biology , 5 ( 3 ): e77 , https://doi.org/10.1371/journal.pbio.0050077 https://doi.org/10.1371/journal.pbio.0050077 .
Schäfer H , Abbas B , Witte H et al . 2002 . Genetic diversity of 'satellite' bacteria present in cultures of marine diatoms . FEMS Microbiology Ecology , 42 ( 1 ): 25 - 35 , https://doi.org/10.1111/j.1574-6941.2002.tb00992.x https://doi.org/10.1111/j.1574-6941.2002.tb00992.x .
Segata N , Izard J , Waldron L et al . 2011 . Metagenomic biomarker discovery and explanation . Genome Biology , 12 ( 6 ): R60 , https://doi.org/10.1186/gb-2011-12-6-r60 https://doi.org/10.1186/gb-2011-12-6-r60 .
Simonato F , Gómez-Pereira P R , Fuchs B M et al . 2010 . Bacterioplankton diversity and community composition in the Southern Lagoon of Venice . Systematic and Applied Microbiology , 33 ( 3 ): 128 - 138 , https://doi.org/10.1016/j.syapm.2009.12.006 https://doi.org/10.1016/j.syapm.2009.12.006 .
Sohn J H , Lee J H , Yi H N et al . 2004 . Kordia algicida gen. nov., sp. nov., an algicidal bacterium isolated from red tide . International Journal of Systematic and Evolutionary Microbiology , 54 ( 3 ): 675 - 680 , https://doi.org/10.1099/ijs.0.02689-0 https://doi.org/10.1099/ijs.0.02689-0 .
Stat M , Pochon X , Franklin E C et al . 2013 . The distribution of the thermally tolerant symbiont lineage ( Symbiodinium clade D) in corals from Hawaii: correlations with host and the history of ocean thermal stress . Ecology and Evolution , 3 ( 5 ): 1317 - 1329 , https://doi.org/10.1002/ece3.556 https://doi.org/10.1002/ece3.556 .
Struszczyk H , Pospieszny H . 1997 . New Applications of Chitinand Its Derivatives in Plant Protection. CRC Press . Boca Raton, Florida , 14p .
Thomas F , Hehemann J H , Rebuffet E et al . 2011 . Environmental and gut Bacteroidetes : the food connection . Frontiers in Microbiology , 2 : 93 , https://doi.org/10.3389/fmicb.2011.00093 https://doi.org/10.3389/fmicb.2011.00093 .
Tujula N A , Crocetti G R , Burke C et al . 2010 . Variability and abundance of the epiphytic bacterial community associated with a green marine Ulvacean alga . The ISME Journal , 4 ( 2 ): 301 - 311 , https://doi.org/10.1038/ismej.2009.107 https://doi.org/10.1038/ismej.2009.107 .
Venter J C , Remington K , Heidelberg J F et al . 2004 . Environmental genome shotgun sequencing of the Sargasso Sea . Science , 304 ( 5667 ): 66 - 74 , https://doi.org/10.1126/science.1093857 https://doi.org/10.1126/science.1093857 .
Wagner M R , Lundberg D S , Coleman-Derr D et al . 2014 . Natural soil microbes alter flowering phenology and the intensity of selection on flowering time in a wild Arabidopsis relative . Ecology Letters , 17 ( 6 ): 717 - 726 , https://doi.org/10.1111/ele.12276 https://doi.org/10.1111/ele.12276 .
Wagner-Döbler I , Ballhausen B , Berger M et al . 2010 . The complete genome sequence of the algal symbiont Dinoroseobacter shibae : a hitchhiker's guide to life in the sea . The ISME Journal , 4 ( 1 ): 61 - 77 , https://doi.org/10.1038/ismej.2009.94 https://doi.org/10.1038/ismej.2009.94 .
Wang W J , Sun X T , Liu F L et al . 2016 . Effect of abiotic stress on the gameophyte of Pyropia katadae var. hemiphylla (Bangiales, Rhodophyta) . Journal of Applied Phycology , 28 ( 1 ): 469 - 479 , https://doi.org/10.1007/s10811-015-0579-4 https://doi.org/10.1007/s10811-015-0579-4 .
Yoshida T , Notoya M , Kikuchi N et al . 1997 . Catalogue of species of Porphyra in the world, with special reference to the type locality and bibliography . Natural History Research. , 3 : 5 - 18 .
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