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Diversity of the epiphytic bacterial communities associated with commercially cultivated healthy and diseased Saccharina japonica during the harvest season

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Abstract

Disease outbreaks cause severe economic losses in commercially cultivated Saccharina japonica. Epiphytic bacteria are increasingly recognized to play an important role in S. japonica health and may also become opportunistic pathogens when the environment deteriorates. However, there is little knowledge about the epiphytic bacterial communities associated with commercially cultivated S. japonica and how these communities change over the harvest season. We analyzed the diversity, composition, and temporal dynamics of epiphytic bacterial communities associated with both healthy and diseased tissue of S. japonica over a harvest season (from April to June, 2015) at Ailian Bay, Rongcheng, China. Our results showed that Proteobacteria and Bacteroidetes were the main phyla and Halomonas spp. were the most dominant bacterial species. Halomonadaceae, Hyphomonadaceae, Rhodobacteraceae, and Phyllobacteriaceae families were abundant in both healthy and diseased S. japonica, but the relative abundance of these bacteria differed between healthy and diseased groups. Spatial (site 1, site 2, and site 3 in April) and temporal comparisons (site 3 from April to June) revealed that the bacterial community associated with cultivated S. japonica was influenced by sampling time and sampling site independent of the health status. Several OTUs from the Roseobacter group, including members of the genera Sulfitobacter and Loktanella, were enriched in diseased tissues suggesting these taxa could be candidate opportunistic pathogens. In contrast, OTUs belonging to the genera Halomonas were enriched in healthy tissues, indicating a potential beneficial role for group during the cultivation of S. japonica. Our results provide important baseline knowledge of the epiphytic bacterial communities and possibly pathogenic bacteria associated with commercially cultivated S. japonica.

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References

  • Abraham WR, Rohde M (2014) The family Hyphomonadaceae. In: Rosenberg E, DeLong EF, Lory S, Stackebrandt E, Thompson F (eds) The prokaryotes: Alphaproteobacteria and Betaproteobacteria, 4rd edn. Springer, Heidelberg, pp 283–299

    Google Scholar 

  • Barott KL, Rodriguez-Brito B, Janouškovec J, Marhaver KL, Smith JE, Keeling P, 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

    CAS  PubMed  Google Scholar 

  • Bengtsson MM, Sjøtun K, Øvreås L (2010) Seasonal dynamics of bacterial biofilms on the kelp Laminaria hyperborea. Aquat Microb Ecol 60:71–83

    Google Scholar 

  • Bengtsson MM, Sjøtun K, Lanzén A, Øvreås L (2012) Bacterial diversity in relation to secondary production and succession on surfaces of the kelp Laminaria hyperborea. ISME J 6:2188–2198

    CAS  PubMed  PubMed Central  Google Scholar 

  • Burke C, Thomas T, Lewis M, Steinberg P, Kjelleberg S (2011) Composition, uniqueness and variability of the epiphytic bacterial community of the green alga Ulva australis. ISME J 5:590–600

    CAS  PubMed  Google Scholar 

  • Campbell AH, Harder T, Nielsen S, Kjelleberg S, Steinberg PD (2011) Climate change and disease: bleaching of a chemically defended seaweed. Glob Chang Biol 17:2958–2970

    Google Scholar 

  • Campbell AM, Fleisher J, Sinigalliano C, White JR, Lopez JV (2015) Dynamics of marine bacterial community diversity of the coastal waters of the reefs, inlets, and wastewater outfalls of southeast Florida. MicrobiologyOpen 4:390–408

    CAS  PubMed  PubMed Central  Google Scholar 

  • Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Peña AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Turnbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336

    CAS  PubMed  PubMed Central  Google Scholar 

  • Case RJ, Longford SR, Campbell AH, Low A, Tujula N, Steinberg PD, Kjelleberg S (2011) Temperature induced bacterial virulence and bleaching disease in a chemically defended marine macroalga. Environ Microbiol 13:529–537

    CAS  PubMed  Google Scholar 

  • Chen D, Lin G, Shen S (1979) Studies on alginic acid decomposing bacteria I. Action of alginic acid decomposing bacteria and alginase on Laminaria japonica. Oceanol Limnol Sin 10:329–333

  • Chen D, Lin G, Shen S (1981) Studies on alginic acid decomposing bacteria II. Rot disease of Laminaria summer sporelings caused by alginic acid decomposing bacteria. Oceanol Limnol Sin 12:133–137

    Google Scholar 

  • Chen D, Liu X, Liu X, Yu Y, Yang Z, Qui S (1983) Studies on alginic acid-decomposing bacteria. III. The cause of rot disease and detaching of Laminaria sporophytes in sporeling culture stations and their preventive measures. Oceanol Limnol Sin 15:581–589

    Google Scholar 

  • Chen D, Liu X, Liu X, Wang Q (1986) Studies on alginic acid decomposing bacteria IV. Distribution of alginic acid decomposing bacteria in Laminaria farm and its ecological significance. Oceanol Limnol Sin 17:137–143

    Google Scholar 

  • Collén J, Porcel B, Carré W, Ball SG, Chaparro C, Tonon T, Barbeyron T, Michel G, Noel B, Valentin K, Elias M, Artiguenave F, Arun A, Aury JM, Barbosa-Neto JF, Bothwell JH, Bouget FY, Brillet L, Cabello-Hurtado F, Capella-Gutiérrez S, Charrier B, Cladière L, Cock JM, Coelho SM, Colleoni C, Czjzek M, Silva CD, Delage L, Denoeud F, Deschamps P, Dittami SM, Gabaldón T, Gachon CM, Groisillier A, Hervé C, Jabbari K, Katinka M, Kloareg B, Kowalczyk N, Labadie K, Leblanc C, Lopez PJ, McLachlan DH, Meslet-Cladiere L, Moustafa A, Nehr Z, Collén PN, Panaud O, Partensky F, Poulain J, Rensing SA, Rousvoal S, Samson G, Symeonidi A, Weissenbach J, Zambounis A, Wincker P, Boyen C (2013) Genome structure and metabolic features in the red seaweed Chondrus crispus shed light on evolution of the Archaeplastida. Proc Natl Acad Sci U S A 110:5247–5252

    PubMed  PubMed Central  Google Scholar 

  • Croft MT, Lawrence AD, Raux-Deery E, Warren MJ, Smith AG (2005) Algae acquire vitamin B12 through a symbiotic relationship with bacteria. Nature 438:90–93

    CAS  PubMed  Google Scholar 

  • DeSantis TZ, Hugenholtz P, Larsen N, Rojas M, Brodie EL, Keller K, Huber T, Dalevi D, Hu P, Andersen GL (2006) Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl Environ Microbiol 72:5069–5072

    CAS  PubMed  PubMed Central  Google Scholar 

  • Edgar RC (2013) UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods 10:996–998

    CAS  PubMed  Google Scholar 

  • Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27:2194–2200

    CAS  PubMed  PubMed Central  Google Scholar 

  • Egan S, Gardiner M (2016) Microbial dysbiosis: rethinking disease in marine ecosystems. Front Microbiol 7:991

    PubMed  PubMed Central  Google Scholar 

  • Egan S, Fernandes ND, Kumar V, Gardiner M, Thomas T (2014) Bacterial pathogens, virulence mechanism and host defence in marine macroalgae. Environ Microbiol 16:925–938

    CAS  PubMed  Google Scholar 

  • Fernandes N, Case RJ, Longford SR, Seyedsayamdost MR, Steinberg PD, Kjelleberg S, Thomas T (2011) Genomes and virulence factors of novel bacterial pathogens causing bleaching disease in the marine red alga Delisea pulchra. PLoS One 6:e27387

    CAS  PubMed  PubMed Central  Google Scholar 

  • Goecke F, Labes A, Wiese J, Imhoff JF (2010) Chemical interactions between marine macroalgae and bacteria. Mar Ecol Prog Ser 409:267–299

    CAS  Google Scholar 

  • Goecke F, Labes A, Wiese J, Imhoff JF (2012) Dual effect of macroalgal extracts on growth of bacteria in Western Baltic Sea. Rev Biol Mar Oceanogr 47:7586

    Google Scholar 

  • Hollants J, Leliaert F, De Clerck O, Willems A (2013) What we can learn from sushi: a review on seaweed-bacterial associations. FEMS Microbiol Ecol 83:1–16

    CAS  PubMed  Google Scholar 

  • Ivanova EP, Bakunina IY, Sawabe T, Hayashi K, Alexeeva YV, Zhukova NV, Nicolau DV, Zvaygintseva TN, Mikhailov VV (2002) Two species of culturable bacteria associated with degradation of brown algae Fucus evanescens. Microb Ecol 43:242–249

    CAS  PubMed  Google Scholar 

  • Kim KK, Lee JS, Stevens DA (2013) Microbiology and epidemiology of Halomonas species. Future Microbiol 8:1559–1573

    CAS  PubMed  Google Scholar 

  • KleinJan H, Jeanthon C, Boyen C, Dittami SM (2017) Exploring the cultivable Ectocarpus microbiome. Front Microbiol 8:2456

    PubMed  PubMed Central  Google Scholar 

  • Kumar V, Zozaya-Valdes E, Kjelleberg S, Thomas T, Egan S (2016) Multiple opportunistic pathogens can cause a bleaching disease in the red seaweed Delisea pulchra. Environ Microbiol 18:3962–3975

    CAS  PubMed  Google Scholar 

  • Lemay MA, Martone PT, Keeling PJ, Burt JM, Krumhansl KA, Sanders RD, Wegener PL (2018) Sympatric kelp species share a large portion of their surface bacterial communities. Environ Microbiol 20:658–670

    PubMed  Google Scholar 

  • Lin W, Zhang W, Yan X, Duan D (2004) Distribution and reinfection of alginic acid decomposing bacteria on juvenile Laminaria japonica. Oceanol Limnol Sin 35:562–567

    Google Scholar 

  • Liu C, Wang L, Wang M, Tang X (2002) Difference analysis of infection activity of alginic acid decomposing bacteria infecting Laminaria japonica. Mar Sci 26:44–47

    CAS  Google Scholar 

  • Mancuso FP, D’hondt S, Willems A, Airoldi L, De Clerck O (2016) Diversity and temporal dynamics of the epiphytic bacterial communities associated with the canopy-forming seaweed Cystoseira compressa (Esper) Gerloff and Nizamuddin. Front Microbiol 7:476

    PubMed  PubMed Central  Google Scholar 

  • Marzinelli EM, Campbell AH, Zozaya Valdes E, Vergés A, Nielsen S, Wernberg T, de Bettignies T, Bennett S, Caporaso JG, Thomas T, Steinberg PD (2015) Continental-scale variation in seaweed host-associated bacterial communities is a function of host condition, not geography. Environ Microbiol 17:4078–4088

    PubMed  Google Scholar 

  • Miranda LN, Hutchison K, Grossman AR, Brawley SH (2013) Diversity and abundance of the bacterial community of the red macroalga Porphyra umbilicalis: did bacterial farmers produce macroalgae? PLoS One 8:e58269

    CAS  PubMed  PubMed Central  Google Scholar 

  • Poindexter JS (2006) Dimorphic prosthecate bacteria: the genera Caulobacter, Asticcacaulis, Hyphomicrobium, Pedomicrobium, Hyphomonas and Thiodendron. In: Dworkin M, Falkow S, Rosenberg E, Schleifer KH, Stackebrandt E (eds) The prokaryotes. Springer, New York, pp 72–90

    Google Scholar 

  • Sawabe T, Tanaka R, Iqbal MM, Tajima K, Ezura Y, Ivanova EP, Christen R (2000) Assignment of Alteromonas elyakovii KMM 162T and five strains isolated from spot-wounded fronds of Laminaria japonica to Pseudoalteromonas elyakovii comb. nov. and the extended description of the species. Int J Syst Evol Microbiol 50:265–271

    CAS  PubMed  Google Scholar 

  • Singh RP (2013) Studies on certain seaweed-bacterial interaction from Saurashtra coast. Dissertation, Maharaja Krishnakumarsinhji Bhavnagar University

  • Singh RP, Reddy C (2014) Seaweed–microbial interactions: key functions of seaweed-associated bacteria. FEMS Microbiol Ecol 88:213–230

    CAS  PubMed  Google Scholar 

  • Singh RP, Mantri VA, Reddy C, Jha B (2011) Isolation of seaweed-associated bacteria and their morphogenesis-inducing capability in axenic cultures of the green alga Ulva fasciata. Aquat Biol 12:13–21

    Google Scholar 

  • Spoerner M, Wichard T, Bachhuber T, Stratmann J, Oertel W (2012) Growth and thallus morphogenesis of Ulva mutabilis (Chlorophyta) depends on a combination of two bacterial species excreting regulatory factors. J Phycol 48:1433–1447

    PubMed  Google Scholar 

  • Staufenberger T, Thiel V, Wiese J, Imhoff JF (2008) Phylogenetic analysis of bacteria associated with Laminaria saccharina. FEMS Microbiol Ecol 64:65–77

    CAS  PubMed  Google Scholar 

  • Sunagawa S, DeSantis TZ, Piceno YM, Brodie EL, DeSalvo MK, Voolstra CR, Weil E, Andersen GL, Medina M (2009) Bacterial diversity and White plague disease-associated community changes in the Caribbean coral Montastraea faveolata. ISME J l 3:512–521

    CAS  Google Scholar 

  • Tang J, Xiao Y, Oshima A, Kawai H, Nagata S (2008) Disposal of seaweed wakame (Undaria pinnatifida) in composting process by marine bacterium Halomonas sp. AW4. Int J Biotechnol 10:73–85

    Google Scholar 

  • Tang J, Wang M, Zhou Q, Nagata S (2011) Improved composting of undaria pinnatifida seaweed by inoculation with Halomonas and Gracilibacillus sp. isolated from marine environments. Bioresour Technol 102:2925–2930

    CAS  PubMed  Google Scholar 

  • Tapia JE, González B, Goulitquer S, Potin P, Correa J (2016) Microbiota influences morphology and reproduction of the brown alga Ectocarpus sp. Front Microbiol 7:197

    PubMed  PubMed Central  Google Scholar 

  • Tseng C (1994) Anthology of Tseng Cheng-Kui. Ocean Press, Beijing

    Google Scholar 

  • Wang Y, Tang X, Yang Z (2003a) Screening of alginic acid decomposing bacteria and its culture conditions. J Fish Sci China 10:51–54

    Google Scholar 

  • Wang L, Tang X, Wang M, Zhang P (2003b) The roles played by alginic acid decomposing bacteria during the time of green decay disease of Laminaria japonica. J Ocean Univ Qingdao 33:245–248

    Google Scholar 

  • Wang G, Shuai L, Li Y, Lin W, Zhao X, Duan D (2008) Phylogenetic analysis of epiphytic marine bacteria on hole-rotten diseased sporophytes of Laminaria japonica. J Appl Phycol 20:403–409

    Google Scholar 

  • Wang G, Lu B, Shuai L, Li D, Zhang R (2014) Microbial diseases of nursery and field-cultivated Saccharina japonica (Phaeophyta) in China. Algol Stud 145/146, 2: 39-51

  • Weigel B, Pfister CA (2019) Successional dynamics and seascape-level patterns of microbial communities on the canopy-forming kelps Nereocystis luetkeana and Macrocystis pyrifera. Front Microbiol 10:00346

  • Weiner RM, Melick M, O’Neill K, Quintero E (2000) Hyphomonas adhaerens sp. nov., Hyphomonas johnsonii sp. nov. and Hyphomonas rosenbergii sp. nov. marine budding and prosthecate bacteria. Int J Syst Evol Microbiol 50:459–469

    CAS  PubMed  Google Scholar 

  • Wong TY, Preston LA, Schiller NL (2000) Alginate lyase: review of major sources and enzyme characteristics, structure-function analysis, biological roles, and applications. Annu Rev Microbiol 54:289–340

    CAS  PubMed  Google Scholar 

  • Wu C (1990) Cultivation of temperate seaweeds in the Asia Pacific region. In: Regional Workshop on the Culture and Utilization of Seaweeds, Cebu City, Philippines. http://www.fao.org/3/ab728e/AB728E02.htm#ch2

  • Xiang J (2001) Disease occurrence and control strategies of mariculture organisms. Ocean Press, Beijing, pp 78–83

    Google Scholar 

  • Zozaya-Valdes E, Egan S, Thomas T (2015) A comprehensive analysis of the microbial communities of healthy and diseased marine macroalgae and the detection of known and potential bacterial pathogens. Front Microbiol 6:146

    PubMed  PubMed Central  Google Scholar 

Download references

Funding

This study was sponsored by the Marine S & T Fund of Shandong Province for Pilot National Laboratory for Marine Science and Technology (Qingdao) (2018SDKJ0406-5), the National Natural Science Foundation of China (41576158), the Fundamental Research Funds for the Central Universities (3005000-84-1822025), and the Student Research Training Program of Ocean University of China (201210423048).

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Authors and Affiliations

  1. College of Marine Life Sciences, Ocean University of China, Qingdao, 266003, China

    Rui Zhang, Xiaoyang Zhang, Qi Han, Nan Li & Gaoge Wang

  2. Institute of Evolution & Marine Biodiversity, Ocean University of China, Qingdao, 266003, China

    Rui Zhang, Xiaoyang Zhang, Qi Han & Gaoge Wang

  3. Weihai Changqing Ocean Science & Technology Co., Ltd, Rongcheng, 264316, China

    Lirong Chang & Luyang Xiao

  4. Key Laboratory of Molecular Virology and Immunology, Institute Pasteur of Shanghai, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, University of Chinese Academy of Sciences, Shanghai, 200031, China

    Nan Li

  5. Centre for Marine Science and Innovation & School of Biological, Earth and Environmental Sciences, The University of New South Wales, Sydney, NSW, 2052, Australia

    Suhelen Egan

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  1. Rui Zhang
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Zhang, R., Chang, L., Xiao, L. et al. Diversity of the epiphytic bacterial communities associated with commercially cultivated healthy and diseased Saccharina japonica during the harvest season. J Appl Phycol 32, 2071–2080 (2020). https://doi.org/10.1007/s10811-019-02025-y

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