Skip to main content
SpringerLink
Log in

Bacterial community temporal dynamics and disease-related variations in the seawater of Pyropia (laver) seedling pools

  • Published:
Journal of Applied Phycology Aims and scope Submit manuscript

Abstract

Conchocelis cultivation is a crucial step in the industrial growth of Pyropia (laver). However, our knowledge of the seawater microbiology community in Pyropia seedling pools is limited. This study investigated the temporal dynamics in seedling pool microbiota before and after outbreaks of yellow spot disease in Pyropia yezoensis conchocelis. A total of 18 water samples were collected to assess seedling pool health status, followed by the sequencing of microbiota 16S ribosomal RNA (rRNA). Analysis of 16,760,224 16S rRNA gene sequences indicated that the core microbe group comprised 207 genera. The microbial diversity of samples gradually increased from May to July. The bacterial diversity of seawater samples from diseased P. yezoensis seedling pools was significantly higher than samples from healthy seedling pools. It is noteworthy that each pool group had a distinctive microbial community composition. The relative abundance of two dominant bacteria genera, Sediminicola and Roseivirga, increased over time in healthy seedling pools, peaking in August, while Vibrio remained at constantly low levels. However, the abundance of Vibrio and Polaribacter increased sharply in diseased P. yezoensis seedling pools and decreased after fresh seawater exchange. This indicates that these bacteria are probably associated with the filament disease. Many disease-associated bacteria are negatively related to the HCO3 − concentration in seawater and positively related to pH. Changes in bacteria and environmental factors reflect the characteristics of microbial community succession in seedling pools and therefore have potential to be used as biomarkers and environmental signals for Pyropia disease monitoring.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Bartram AK, Lynch MDJ, Stearns JC, Moreno-Hagelsieb G, Neufeld JD (2011) Generation of multimillion-sequence 16S rRNA gene libraries from complex microbial communities by assembling paired-end illumina reads. Appl Environ Microbiol 77:3846–3852

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Blouin NA, Brodie JA, Grossman AC, Xu P, Brawley SH (2011) Porphyra: a marine crop shaped by stress. Trends Plant Sci 16:29–37

    Article  CAS  PubMed  Google Scholar 

  • Caporaso JG et al (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Meth 7:335–336

    Article  CAS  Google Scholar 

  • Chen CS, Ji DH, Yao H, Huang SY, Zheng WG (2004) Comparison of growth and development among four series of different living conchocelis of Porphyra haitanensis in transnormal surroundings. J Oceanogr Taiwan Strait 23:489–495

    CAS  Google Scholar 

  • DeSantis TZ et al (2006) Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl Environ Microbiol 72:5069–5072

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Drew KM (1949) Conchocelis-phase in the life-history of Porphyra umbilicalis (L.) Kütz. Nature 164:748–749

    Article  Google Scholar 

  • Fernandes N, Steinberg P, Rusch D, Kjelleberg S, Thomas T (2012) Community structure and functional gene profile of bacteria on healthy and diseased thalli of the red seaweed Delisea pulchra. PLoS One 7:e50854

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fu CH, Yan XH, Huang LB, Li L (2011) The releasing and hightemperature resistance of conchospores from an improved strain in Porphyra yezoensis Ueda (Bangiales, Rhodophyta). Oceanol Limnol Sinica 42:460–466

    Google Scholar 

  • Fujita Y (1990) Diseases of cultivated Porphyra in Japan. In: Akatsuka (eds) Introduction to Applied Phycology: SPB Academic Publishing, The Hague, pp 177-190

  • Green LA, Neefus CD (2015) Effects of temperature, light level, photoperiod, and ammonium concentration on Pyropia leucosticta (Bangiales, Rhodophyta) from the Northwest Atlantic. J Appl Phycol 27:1253–1261

    Article  CAS  Google Scholar 

  • Guan X, Li J, Zhang Z, Li F, Yang R (2013) Characterizing the microbial culprit of white spot disease of the conchocelis stage of Porphyra yezoensis (Bangiales, Rhodophyta). J Appl Phycol 25:1341–1348

    Article  CAS  Google Scholar 

  • Huson DH, Auch AF, Qi J, Schuster SC (2007) MEGAN analysis of metagenomic data. Genome Res 17:377–386

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim GH, Moon KH, Kim JY, Shim J, Klochkova TA (2014) A revaluation of algal diseases in Korean Pyropia (Porphyra) sea farms and their economic impact. Algae 29:249–265

    Article  Google Scholar 

  • Kim GH, Klochkova TA, Da JL, Im SH (2016) Chloroplast virus causes green-spot disease in cultivated Pyropia of Korea. Algal Res 17:293–299

    Article  Google Scholar 

  • Kowalenko CG, Yu S (1996) Solution, exchangeable and clay-fixed ammonium in south coast British Columbia soils. Can J Soil Sci 76:473–483

    Article  CAS  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

    Article  CAS  PubMed  Google Scholar 

  • Lau SC et al (2006) Description of Fabibacter halotolerans gen. nov., sp. nov. and Roseivirga spongicola sp. nov., and reclassification of [Marinicola] seohaensis as Roseivirga seohaensis comb. nov. Int J Syst Evol Microbiol 56:1059–1065

    Article  CAS  PubMed  Google Scholar 

  • Lavilla-Pitogo CR (1992) Agar-digesting bacteria associated with ‘rotten thallus syndrome’ of Gracilaria sp. Aquaculture 102:1–7

    Article  Google Scholar 

  • Luo QJ, Zhu ZG, Zhu ZJ, Yang R, Qian FJ, Chen HM, Yan XJ (2014) Different responses to heat shock stress revealed heteromorphic adaptation strategy of Pyropia haitanensis (Bangiales, Rhodophyta). Plos One 9(4):e94354

  • Magoc T, Salzberg SL (2011) FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27:2957–2963

    Article  CAS  PubMed  PubMed Central  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

    Article  PubMed  PubMed Central  Google Scholar 

  • Martinez JN, Padilla PI (2016) Isolation and characterization of agar-digesting Vibrio species from the rotten thallus of Gracilariopsis heteroclada Zhang et Xia. Mar Env Res 119:156–160

    Article  CAS  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nedashkovskaya OI et al (2005a) Roseivirga ehrenbergii gen. nov., sp. nov., a novel marine bacterium of the phylum ‘Bacteroidetes’, isolated from the green alga Ulva fenestrata. Int J Systemat Evol Microbiol 55:231–234

    Article  CAS  Google Scholar 

  • Nedashkovskaya OI, Kim SB, Lysenko AM, Park MS, Mikhailov VV, Bae KS, Park HY (2005b) Roseivirga echinicomitans sp. nov., a novel marine bacterium isolated from the sea urchin Strongylocentrotus intermedius, and emended description of the genus Roseivirga. Int J Systemat Evol Microbiol 55:1797–1800

    Article  CAS  Google Scholar 

  • Taniguchi M (1977a) Strdies on the yellow spot disease in conchocelis-III: aquatic factors influencing the development of the yellow spot disease. Bull Jap Soc Sci Fish 43:259–263

    Article  Google Scholar 

  • Taniguchi M (1977b) Studies on the yellow spot disease in conchocelis-II: method for obtaining the pathogen complex. Bull Jap Soc Sci Fish 43:255–258

    Article  Google Scholar 

  • Tseng CK (1981) Commercial cultivation. In: Lobban CS, Wynne MJ (eds) The Biology of Seaweeds pp 687-725

  • Waaland JR, Dickson LG, Duffield ECS (1990) Conchospore production and seasonal occurrence of some Porphyra species (Bangiales, Rhodophyta) in Washington state. Hydrobiologia 204(205):453–459

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Wang HB, Li XS, Xia YM, Yan BL (2011) Isolation, identification and biological pathogen of yellow spot disease in conchocelis of Porphyra yezoensis. Mar Env Sci 30:361–364

    Google Scholar 

  • Watanabe Y, Nishihara GN, Tokunaga S, Terada R (2014) Effect of irradiance and temperature on the photosynthesis of a cultivated red alga, Pyropia tenera (= Porphyra tenera), at the southern limit of distribution in Japan. Phycol Res 62:187–196

    Article  CAS  Google Scholar 

  • Wells ML, Potin P, Craigie JS, Raven JA, Merchant SS, Helliwell KE, Smith AG, Camire ME, Brawley SH (2017) Algae as nutritional and functional food sources: revisiting our understanding. J Appl Phycol 29(2):949–982

    Article  CAS  PubMed  Google Scholar 

  • Zhong Z, Wang W, Sun X, Liu F, Liang Z, Wang F, Chen W (2016) Developmental and physiological properties of Pyropia dentata (Bangiales, Rhodophyta) conchocelis in culture. J Appl Phycol 28:3435–3445

    Article  Google Scholar 

Download references

Acknowledgements

This research was supported by the Fundamental Research Funds for the Central Universities (grant no. 2652015166 to XG), the Jiangsu Science and Technology Infrastructure Construction Project (grant no. BM2015017) and the Jiangsu Agriculture Science and Technology Innovation Fund (grant no. CX(16)1018 to QL), and the Nantong Science and Technology Project (grant no. MS12015068 to CH). The authors are particularly grateful to Lingling Hou and Fei Liu for their assistance with 16S rRNA sequencing and water quality monitoring.

Author information

Authors and Affiliations

  1. School of Ocean Sciences, China University of Geosciences, Beijing, 100083, China

    Xiangyu Guan & Xiaoxuan Zheng

  2. Marine Fisheries Institute of Jiangsu Province, Nantong, 226007, China

    Wei Zhou, Chuanming Hu, Miaoxian Zhu, Yaping Ding, Jianyi Zhu & Qinqin Lu

  3. Jiangsu Provincial Platform for Conservation and Agricultural Germplasm, Nanjing, 210014, China

    Wei Zhou, Chuanming Hu, Miaoxian Zhu, Yaping Ding, Jianyi Zhu & Qinqin Lu

  4. School of Life Science, Liaoning Normal University, Dalian, 116081, China

    Shanshan Gai

Authors
  1. Xiangyu Guan
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Wei Zhou
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Chuanming Hu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Miaoxian Zhu
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Yaping Ding
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Shanshan Gai
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Xiaoxuan Zheng
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Jianyi Zhu
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Qinqin Lu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Xiangyu Guan or Qinqin Lu.

Electronic supplementary material

Table S1

(DOCX 24 kb)

Table S2

(DOCX 26 kb)

Table S3

(XLSX 87 kb)

Figure S1

Shell-boring conchocelis suffering yellow-spot disease. (JPEG 289 kb)

Figure S2

Data size of each sample group (mean ± SD). (PDF 265 kb)

Figure S3

Length distribution of all sequences merged from paired-end reads. Paired-end reads were merged into a long sequence according to the overlap of each pair of reads.(PDF 172 kb)

Figure S4

Estimated coverage of sequencing based on OTU observations (97% similarity). (PDF 170 kb)

Figure S5

Shared and unique bacterial genera in healthy seedling pools. (PDF 493 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Guan, X., Zhou, W., Hu, C. et al. Bacterial community temporal dynamics and disease-related variations in the seawater of Pyropia (laver) seedling pools. J Appl Phycol 30, 1217–1224 (2018). https://doi.org/10.1007/s10811-017-1272-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10811-017-1272-6

Keywords

Search

Navigation