Chemical interactions between kelp Macrocystis pyrifera and symbiotic bacteria under elevated CO2 condition

Xiaowen Zhang , Tianle Xi , Yitao Wang , Xiao Fan , Dong Xu , Pengyan Zhang , Ke Sun , Yan Zhang , Jian Ma , Naihao Ye

Marine Life Science & Technology ›› : 1 -13.

PDF
Marine Life Science & Technology ›› : 1 -13. DOI: 10.1007/s42995-024-00259-5
Research Paper

Chemical interactions between kelp Macrocystis pyrifera and symbiotic bacteria under elevated CO2 condition

Author information +
History +
PDF

Abstract

Kelps are pivotal to temperate coastal ecosystems, providing essential habitat and nutrients for diverse marine life, and significantly enhancing local biodiversity. The impacts of elevated CO2 levels on kelps may induce far-reaching effects throughout the marine food web, with potential consequences for biodiversity and ecosystem functions. This study considers the kelp Macrocystis pyrifera and its symbiotic microorganisms as a holistic functional unit (holobiont) to examine their collective response to heightened CO2 levels. Over a 4 month cultivation from the fertilization of M. pyrifera gametes to the development of juvenile sporophytes, our findings reveal that elevated CO2 levels influence the structure of the M. pyrifera symbiotic microbiome, alter metabolic profiles, and reshape microbe-metabolite interactions using 16S rRNA amplicon sequencing and liquid chromatography coupled to mass spectrometry analysis. Notably, Dinoroseobacter, Sulfitobacter, Methylotenera, Hyphomonas, Milano-WF1B-44 and Methylophaga were selected as microbiome biomarkers, which showed significant increases in comparative abundance with elevated CO2 levels. Stress-response molecules including fatty-acid metabolites, oxylipins, and hormone-like compounds such as methyl jasmonate and prostaglandin F2a emerged as critical metabolomic indicators. We propose that elevated CO2 puts certain stress on the M. pyrifera holobiont, prompting the release of these stress-response molecules. Moreover, these molecules may aid the kelp’s adaptation by modulating the microbial community structure, particularly influencing potential pathogenic bacteria, to cope with environmental change. These results will enrich the baseline data related to the chemical interactions between the microbiota and M. pyrifera and provide clues for predicting the resilience of kelps to future climate change.

Keywords

Kelp / Holobiont / Elevated CO2 / Microbiome / Metabolome

Cite this article

Download citation ▾
Xiaowen Zhang, Tianle Xi, Yitao Wang, Xiao Fan, Dong Xu, Pengyan Zhang, Ke Sun, Yan Zhang, Jian Ma, Naihao Ye. Chemical interactions between kelp Macrocystis pyrifera and symbiotic bacteria under elevated CO2 condition. Marine Life Science & Technology 1-13 DOI:10.1007/s42995-024-00259-5

登录浏览全文

4963

注册一个新账户 忘记密码

References

[1]

Adouane E, Mercier C, Mamelle J, Willocquet E, Intertaglia L, Burgunter-Delamare B, Leblanc C, Rousvoal S, Lami R, Prado S. Importance of quorum sensing crosstalk in the brown alga Saccharina latissima epimicrobiome. iScience, 2024, 27: 109176

[2]

Ameye M, Allmann S, Verwaeren J, Smagghe G, Haesaert G, Schuurink RC, Audenaert K. Green leaf volatile production by plants: a meta-analysis. New Phytol, 2017, 220: 666-683

[3]

Bolyen E, Rideout JR, Dillon MR, Bokulich NA, Abnet CC, Al-Ghalith GA, Alexander H, Alm EJ, Arumugam M, Asnicar F, Bai Y, Bisanz JE, Bittinger K, Brejnrod A, Brislawn CJ, Brown CT, Callahan BJ, Caraballo-Rodríguez AM, Chase J, Cope EK, et al. Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nat Biotechnol, 2019, 37: 852-857

[4]

Bulgarelli D, Rott M, Schlaeppi K, Themaat EV, Ahmadinejad N, Assenza F, Rauf P, Huettel B, Reinhardt R, Schmelzer E, Peplies J, Gloeckner FO, Amann R, Eickhorst T, Schulze-Lefert P. Revealing structure and assembly cues for Arabidopsis root-inhabiting bacterial microbiota. Nature, 2012, 488: 91-95

[5]

Burgunter-Delamare B, Rousvoal S, Legeay E, Tanguy G, Fredriksen S, Boyen C, Dittami SM. The Saccharina latissima microbiome: effects of region, season, and physiology. Front Microbiol, 2022, 13: 1050939

[6]

Callahan BJ, McMurdie PJ, Rosen MJ, Han AW, Johnson AJ, Dada SH. High-resolution sample inference from illumina amplicon data. Nat Methods, 2016, 13: 581-583

[7]

Chen S, Zhou Y, Chen Y, Gu J. Fastp: an ultra-fast all-in-one FASTQ preprocessor. Bioinformatics, 2018, 34: 884-890

[8]

Chen H, Yang R, Chen J, Luo Q, Cui X, Yan X, Gerwick WH. 1-Octen-3-ol, a self-stimulating oxylipin messenger, can prime and induce defense of marine alga. BMC Plant Biol, 2019, 19: 1-16

[9]

Chowdhury MT, Cho J, Ahn DH, Hong Y. Methyl jasmonate enhances phlorotannin production in the brown seaweed Ecklonia cava. J Appl Phycol, 2015, 27: 1651-1656

[10]

Dayton PK. Ecology of kelp communities. Annu Rev Ecol Evol S, 1985, 16: 215-245

[11]

Descamps V, Colin S, Lahaye M, Jam M, Richard C, Potin P, Barbeyron T, Yvin JC, Kloareg B. Isolation and culture of a marine bacterium degrading the sulfated fucans from marine brown algae. Mar Biotechnol, 2006, 8: 27-39

[12]

Dittami SM, Duboscq-Bidot L, Perennou M, Gobet A, Corre E, Boyen C, Tonon T. Host-microbe interactions as a driver of acclimation to salinity gradients in brown algal cultures. ISME J, 2016, 10: 51-63

[13]

Dong S, Yang J, Zhang X, Shi M, Song X, Chen X, Zhang Y. Cultivable alginate lyase-excreting bacteria associated with the arctic brown alga Laminaria. Mar Drugs, 2012, 10: 2481-2491

[14]

Douglas GM, Maffei VJ, Zaneveld JR, Yurgel SN, Brown JR, Taylor CM, Huttenhower C, Langille MG. PICRUSt2 for prediction of metagenome functions. Nat Biotechnol, 2020, 38: 685-688

[15]

Edwards BR, Bidle KD, Van Mooy BA. Dose-dependent regulation of microbial activity on sinking particles by polyunsaturated aldehydes: implications for the carbon cycle. Proc Natl Acad Sci USA, 2015, 112: 5909-5914

[16]

Egan S, Harder T, Burke C, Steinberg P, Kjelleberg S, Thomas T. The seaweed holobiont: understanding seaweed-bacteria interactions. FEMS Microbiol Rev, 2013, 37: 462-476

[17]

Funk CD. Prostaglandins and leukotrienes: advances in eicosanoid biology. Science, 2001, 294: 1871-1875

[18]

Gaitan-Espitia JD, Hancock JR, Padilla-Gamino JL, Rivestb EB, Blanchettec CA, Reedc DC, Hofmann GE. Interactive effects of elevated temperature and pCO2 on early-life history stages of the giant kelp Macrocystis pyrifera. J Exp Mar Biol Ecol, 2014, 457: 51-58

[19]

Gao K, Gao G, Wang Y, Dupont S. Impacts of ocean acidifcation under multiple stressors on typical organisms and ecological processes. Mar Life Sci Tech, 2020, 3: 279-291

[20]

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

[21]

Goulitquer S, Ritter A, Thomas F, Ferec C, Salaün JP, Potin P. Release of volatile aldehydes by the brown algal kelp Laminaria digitata in response to both biotic and abiotic stress. ChemBioChem, 2009, 10: 977-982

[22]

Graham MH, Fox MD, Hamilt SL. Emil O. Macrophyte productivity and the provisioning of energy and habitat to nearshore systems. Marine macrophytes as foundation species, 2016, Boca Raton: CRC Press 133-152

[23]

Harley CD, Randall Hughes A, Hultgren KM, Miner BG, Sorte CJ, Thornber CS, Rodriguez LF, Tomanek L, Williams SL. The impacts of climate change in coastal marine systems. Ecol Lett, 2006, 9: 228-241

[24]

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

[25]

Honkanen T, Jormalainen V. Genotypic variation in tolerance and resistance to fouling in the brown alga Fucus vesiculosus. Oecologia, 2005, 144: 196-205

[26]

Kim HT, Chung JH, Wang D, Lee J, Woo HC, Choi I, Kim KH. Depolymerization of alginate into a monomeric sugar acid using Alg17C, an exo-oligoalginate lyase cloned from Saccharophagus degradans 2–40. Appl Microbiol Biotechnol, 2012, 93: 2233-2239

[27]

Kroeker KJ, Kordas RL, Crim RN, Singh GG. Meta-analysis reveals negative yet variable effects of ocean acidification on marine organisms. Ecol Lett, 2010, 13: 1419-1434

[28]

Kroeker KJ, Kordas RL, Crim RN, Hendriks IE, Ramajo L, Singh GS, Duarte CM, Gattuso JP. Impacts of ocean acidification on marine organisms: quantifying sensitivities and interaction with warming. Glob Change Biol, 2013, 19: 1884-1896

[29]

Kumari P, Reddy CR, Jha B. Methyl jasmonate-induced lipidomic and biochemical alterations in the intertidal macroalga Gracilaria dura (Gracilariaceae, Rhodophyta). Plant Cell Physiol, 2015, 56: 1877-1889

[30]

Küpper FC, Gaquerel E, Cosse A, Adas F, Peters AF, Müller DG, Kloareg B, Salaün JP, Potin P. Free fatty acids and methyl jasmonate trigger defense reactions in Laminaria digitata. Plant Cell Physiol, 2009, 50: 789-800

[31]

Li J, Majzoub ME, Marzinelli EM, Dai Z, Thomas T, Egan S. Bacterial controlled mitigation of dysbiosis in a seaweed disease. ISME J, 2022, 16: 378-387

[32]

Ma M, Zhuang Y, Chang L, Xiao L, Lin Q, Qiu Q, Chen D, Egan S, Wang G. Naturally occurring beneficial bacteria Vibrio alginolyticus X-2 protects seaweed from bleaching disease. Mbio, 2023, 14: e0006523

[33]

Magoč T, Salzberg SL. FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics, 2011, 27: 2957-2963

[34]

Martin M, Barbeyron T, Martin R, Portetelle D, Michel G, Vandenbol M. The cultivable surface microbiota of the brown alga Ascophyllum nodosum is enriched in macroalgal-polysaccharide-degrading bacteria. Front Microbiol, 2015, 6: 1487

[35]

Minich JJ, Morris MM, Brown M, Doane MP, Edwards MS, Michael TP, Dinsdale EA. Elevated temperature drives kelp microbiome dysbiosis, while elevated carbon dioxide induces water microbiome disruption. PLoS ONE, 2018, 13: e0192772

[36]

Oulhen N, Schulz BJ, Carrier TJ. English translation of Heinrich Anton de Bary’s 1878 speech, ‘Die Erscheinung der Symbiose’ (‘De la symbiose’). Symbiosis, 2016, 69: 131-139

[37]

Paix B, Carriot N, Barry-Martinet R, Greff S, Misson B, Briand JF, Culioli G. A multi-omics analysis suggests links between the differentiated surface metabolome and epiphytic microbiota along the thallus of a Mediterranean seaweed holobiont. Front Microbiol, 2020, 11: 513999

[38]

Ren C, Liu Z, Wang X, Qin S. The seaweed holobiont: from microecology to biotechnological applications. Microb Biotechnol, 2022, 15: 738-754

[39]

Ren Y, Yu G, Shi C, Liu L, Guo Q, Han C, Zhang D, Zhang L, Liu B, Gao H, Zeng J, Zhou Y, Qiu Y, Wei J, Luo Y, Zhu F, Li X, Wu Q, Li B, Fu W, et al. Majorbio cloud: a one-stop, comprehensive bioinformatic platform for multiomics analyses. Imeta, 2022, 1: e12

[40]

Roleda MY, Morris JN, McGraw CM, Hurd CL. Ocean acidification and seaweed reproduction: increased CO2 ameliorates the negative effect of lowered pH on meiospore germination in the giant kelp Macrocystis pyrifera (Laminariales, Phaeophyceae). Global Change Biol, 2012, 18: 854-864

[41]

Roth MS, Deheyn DD. Effects of cold stress and heat stress on coral fluorescence in reef-building corals. Sci Rep UK, 2013, 3: 1421

[42]

Sawabe T, Makino H, Tatsumi M, Nakano K, Tajima K, Iqbal MM, Yumoto I, Ezura Y, Christen R. Pseudoalteromonas bacteriolytica sp. nov., a marine bacterium that is the causative agent of red spot disease of Laminaria japonica. Int J Syst Bacteriol, 1998, 48: 769-774

[43]

Scala A, Allmann S, Mirabella R, Haring MA, Schuurinkm RC. Green leaf volatiles: a plant’s multifunctional weapon against herbivores and pathogens. Int J Mol Sci, 2013, 14: 17781-17811

[44]

Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, Sahl JW, Stres B, Thallinger GG, Van Horn D, Weber CF. Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol, 2009, 75: 7537-7541

[45]

Schmidt R, Saha M. Infochemicals in terrestrial plants and seaweed holobionts: current and future trends. New Phytol, 2020, 229: 1852-1860

[46]

Segata N, Izard J, Waldron L, Gevers D, Miropolsky L, Garrett WS, Huttenhower C. Metagenomic biomarker discovery and explanation. Genome Biol, 2011, 12: R60

[47]

Singh RP, Singh RP, Reddy C, Reddy C. Unraveling the functions of the macroalgal microbiome. Front Microbiol, 2016, 6: 1488

[48]

Steneck RS, Graham MH, Bourque BJ, Corbett D, Erlandson JM, Estes JA, Tegner MJ. Kelp forest ecosystems: biodiversity, stability, resilience and future. Environ Conserv, 2002, 29: 436-459

[49]

Stitt M. Rising CO2 levels and their potential significance for carbon flow in photosynthetic cells. Plant Cell Environ, 1991, 14: 741-762

[50]

Vairappan CS, Suzuki M, Motomura T, Ichimura T. Pathogenic bacteria associated with lesions and thallus bleaching symptoms in the Japanese kelp Laminaria religiosa Miyabe (Laminariales, Phaeophyceae). Hydrobiologia, 2001, 445: 183-191

[51]

van der Loos LM, Eriksson BK, Falcão Salles J. The macroalgal holobiont in a changing sea. Trends Microbiol, 2019, 27: 635-650

[52]

Wagner-Döbler I, Ballhausen B, Berger M, Brinkhoff T, Buchholz I, Bunk B, Cypionka H, Daniel R, Drepper T, Gerdts G, Hahnke S, Han C, Jahn D, Kalhoefer D, Kiss H, Klenk H, Kyrpides NC, Liebl W, Liesegang H, Meincke LJ, et al. The complete genome sequence of the algal symbiont Dinoroseobacter shibae: a hitchhiker’s guide to life in the sea. ISME J, 2010, 4: 61-77

[53]

Wahl M, Goecke F, Labes A, Dobretsov S, Weinberger F. The second skin: ecological role of epibiotic biofilms on marine organisms. Front Microbiol, 2012, 3: 31139

[54]

Wang G, Ren Y, Wang S, Hou M, Weinberger F. Shifting chemical defence or novel weapons? A review of defence traits in Agarophyton vermiculophyllum and other invasive seaweeds. Mar Life Sci Technol, 2022, 4: 138-149

[55]

Weber H. Fatty acid-derived signals in plants. Trends Plant Sci, 2002, 7: 217-224

[56]

Weinberger F, Friedlander M. Endogenous and exogenous elicitors of a hypersensitive response in Gracilaria conferta (Rhodophyta). J Appl Phycol, 2000, 12: 139-145

[57]

Westermeier R, Patiño D, Piel MI, Maier I, Müller DG. A new approach to kelp mariculture in Chile: production of free-floating sporophyte seedlings from gametophyte cultures of Lessonia trabeculata and Macrocystis pyrifera. Aquac Res, 2006, 37: 164-171

[58]

Xu D, Wang D, Li B, Fan X, Zhang XW, Ye NH, Wang Y, Mou S, Zhuang Z. Effects of CO2 and seawater acidification on the early stages of Saccharina japonica development. Environ Sci Technol, 2015, 49: 3548-3556

[59]

Zambounis A, Gaquerel E, Strittmatter M, Salaün JP, Potin P, Küpper FC. Prostaglandin A2 triggers a strong oxidative burst in Laminaria: a novel defense inducer in brown algae?. Algae, 2012, 27: 21-32

[60]

Zhang X, Zhang J, Wang Y, Xu D, Fan X, Zhang Y, Ma J, Ye N. The oxylipin messenger 1-octen-3-ol induced rapid responses in kelp Macrocystis pyrifera. Physiol Plant, 2021, 172: 1641-1652

AI Summary AI Mindmap
PDF

405

Accesses

0

Citation

Detail

Sections
Recommended

AI思维导图

/