Skip to main content

Advertisement

Log in

Microbiological degradation of macroalgae waste and its potential considerations for agricultural applications

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

Abstract

The carbon, nitrogen, and phosphate contents of macroalgae suggest their favorable applications for agricultural uses, including soil enrichment through mulching or composting. Macroalgae contain complex and sulfated polysaccharides that are not found in the terrestrial environment and have heterogeneous sugar compositions. The biological process for algae degradation remains undefined. The dominant species of this study include Gracilaria salicornia, Avrainvillea amadelpha, and Acanthophora spicifera. A microbiological community comparison using PCoA analysis with Bray distances determined using the National Institute of Health (NIH) Nephele and Mothur pipeline analysis revealed that the communities between agricultural biomass piles containing terrestrial organic matter (waste biomass—WB1, WB2) were similar, however, distant in relation to the invasive algae pile (algae waste biomass—AWB). Determined using the Geneious software, 27% of the microorganisms in the AWB sample have clear marine origins at the phylogenic family level. Within these identified marine families, 61% have potential algae degradation metabolisms. In addition to the presence of trace metals found in the AWB sample, these are important considerations for agricultural applications.

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

Access this article

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
Fig. 6

Similar content being viewed by others

References

  • Al Abdallah Q, Nixon BT, Fortwendel JR (2016) The enzymatic conversion of major algal and cyanobacterial carbohydrates to bioethanol. Front Energy Res 4:36

  • Alderkamp AC, Van Rijssel M, Bolhuis H (2007) Characterization of marine bacteria and the activity of their enzyme systems involved in degradation of the algal storage glucan laminarin. FEMS Microbiol Ecol 59:108–117

    Article  CAS  PubMed  Google Scholar 

  • Al-Maliki S, Al-Masoudi M (2018) Interactions between Mycorrhizal fungi, tea wastes, and algal biomass affecting the microbial community, soil structure, and alleviating of salinity stress in corn yield (Zea mays L.). Plants 7:63

    Article  CAS  PubMed Central  Google Scholar 

  • Alobwede E, Leake JR, Pandhal J (2019) Circular economy fertilization: testing micro and macro algal species as soil improvers and nutrient sources for crop production in greenhouse and field conditions. Geoderma 334:113–123

    Article  CAS  Google Scholar 

  • Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410

    Article  CAS  PubMed  Google Scholar 

  • Anderson LG, Rocliffe S, Haddayay NR, Dunn AM (2015) The role of tourism and recreation in the spread of non-native species: a systematic review and meta-analysis. PLoS One 10:e014083

    Article  Google Scholar 

  • Baldock JA, Masiello CA, Gelinas Y, Hedges JI (2004) Cycling and composition of organic matter in terrestrial and marine ecosystems. Mar Chem 92:39–64

    Article  CAS  Google Scholar 

  • Basta NT, Ryan JA, Chaney RL (2005) Trace element chemistry in residual-treated soil: key concepts and metal bioavailability. J Environ Qual 34:49–63

    Article  CAS  PubMed  Google Scholar 

  • Battacharyya D, Babgohari MZ, Rathor P, Prithiviraj B (2015) Seaweed extracts as biostimulants in horticulture. Sci Hort 196:39–48

    Article  CAS  Google Scholar 

  • Bax N, Williamson A, Aguero M, Gonzalez E, Geeves W (2003) Marine invasive alien species: a threat to global diversity. Mar Pol 27:313–323

    Article  Google Scholar 

  • Bo S, Lortscher P, Palfery D (2013) Algal biomass anaerobic biodegradability. J Appl Phycol 25:757–761

    Article  CAS  Google Scholar 

  • Boer WD, Folman LB, Summerbell RC, Boddy L (2005) Living in a fungal world: impact of fungi on soil bacterial niche development. FEMS Microbiol Rev 29:795–811

    Article  PubMed  CAS  Google Scholar 

  • Bugg TD, Ahmad M, Hardiman EM, Rahmanpour R (2011) Pathways for degradation of lignin in bacteria and fungi. Nat Prod Rep 28:1883–1896

    Article  CAS  PubMed  Google Scholar 

  • Chapman RL (2013) Algae: the world’s most important “plants”—an introduction. Mitig Adapt Strat Global Change 18:5–12

    Article  Google Scholar 

  • Ciancia M, Matulewics MC, Tuvikene R (2020) Structural diversity in galactans from red seaweeds and its structural influence on rheological properties. Front Plant Sci 11:559986

    Article  PubMed  PubMed Central  Google Scholar 

  • Cole AJ, Roberts DA, Garside AL, de Nys R, Paul NA (2016) Seaweed compost for agricultural crop production. J Appl Phycol 28:629–642

    Article  Google Scholar 

  • De Ramon N'Yeurt A, Iese V (2015) The proliferating brown alga Sargassum polycystum in Tuvalu, South Pacific: assessment of the bloom and applications to local agriculture and sustainable energy. J Appl Phycol 27:2037–2045

    Article  Google Scholar 

  • Dehors J, Mareck A, Kiefer-Meyer MC, Menu-Bouaouiche L, Lehner A, Mollet JC (2019) Evolution of cell wall polymers in tip-growing land plant gametophytes: composition, distribution, functional aspects and their remodeling. Front Plant Sci 10:441

    Article  PubMed  PubMed Central  Google Scholar 

  • Deniaud-Bouët E, Hardouin K, Potin P, Kloareg B, Hervé C (2017) A review about brown algal cell walls and fucose-containing sulfated polysaccharides: cell wall context, biomedical properties and key research challenges. Carbohydr Polym 175:395–408

    Article  PubMed  CAS  Google Scholar 

  • Devault DA, Pierre R, Marfaing H, Dolique F, Lopez P-J (2021) Sargassum contamination and consequences for downstream uses: a review. J Appl Phycol 33:567–602

    Article  Google Scholar 

  • Dorsch M, Lane D, Stackebrandt E (1992) Towards a phylogeny of the genus Vibrio based on 16S rRNA sequences. Int J Syst Evol Microbiol 42:58–63

    CAS  Google Scholar 

  • EPA (1996) Soil Screening guidance: technical background document-Part 5: Chemical- Specific Parameters. EPA Document Number: EPA/540/R-95/128, (May), p. 28 Available at: http://www.epa.gov/superfund/health/conmedia/soil/pdfs/part_5.pdf. Accessed Nov 2019

  • Ficko-Blean E, Préchoux A, Thomas F, Rochat T, Larocque R, Zhu Y, Stam M, Genicot S, Jam M, Calteau A, Viart B, Ropartz D, Perez-Pascual D, Correc G, Matard-Mann M, Stubbs KA, Rogniaux H, Jeudy A, Barbeyron T, Medgue C, Czjzek M, Vallenet D, Mcbride MJ, Dachuaud E, Michel G (2017) Carrageenan catabolism is encoded by a complex regulon in marine heterotrophic bacteria. Nat Commun 8:1–38

    Article  CAS  Google Scholar 

  • Gacesa P (1992) Enzymatic degradation of alginates. Int J Biochem 24:545–552

    Article  CAS  PubMed  Google Scholar 

  • Gorka B, Korzeniowska K, Lipok J, Wieczorek PP (2018) The biomass of algae and algal extracts in agricultural production. In: Chojnacka K, Wieczorek P, Schroeder G, Michalak I (eds) Algae Biomass: Characteristics and Applications. Springer, Cham, pp 103–114

    Chapter  Google Scholar 

  • Gupta MN, Raghava S (2008) Smart systems based on polysaccharides. In: Reis RL, Neves NM, Mano JF, Gomes ME, Marques AP, Azevedo HS (eds) Natural-Based Polymers for Biomedical Applications. Woodhead Publishing, London, pp 129–161

    Chapter  Google Scholar 

  • Han W, Clarke W, Pratt S (2014) Composting of waste algae: a review. Waste Manag 34:1148–1155

    Article  CAS  PubMed  Google Scholar 

  • Henriques B, Rocha LS, Lopes CB, Figueira P, Monteiro RJR, Duarte AC, Pardal MA, Pereira E (2015) Study of bioaccumulation and biosorption of mercury by living marine macroalge: Prospecting for a new remediation biotechnology applied to saline waters. Chem Eng J 281:759–770

    Article  CAS  Google Scholar 

  • Henriques B, Rocha LS, Lopes CB, Figueira P, Duarte AC, Vale C, Pardal MA, Pereira E (2017) A macroalgae based biotechnology for water remediation: simultaneous removal of Cd, Pb, and Hg by living Ulva lactua. J Environ Manag 191:275–289

    Article  CAS  Google Scholar 

  • Illera-Vives M, Seoane Labandeira S, López-Mosquera ME (2013) Production of compost from marine waste: evaluation of the product for use in ecological agriculture. J Appl Phycol 25:1395–1403

    Article  Google Scholar 

  • Imran M, Poduval PB, Ghadi SC (2017) Bacterial degradation of algal polysaccharides in marine ecosystem. In: Naik MM, Dubey SK (eds) Marine Pollution and Microbial Remediation. Springer, Singapore, pp 189–203

    Chapter  Google Scholar 

  • Inderjit, Chapman D, Ranelletti M, Kaushik S (2006) Invasive marine algae: an ecological perspective. Bot Rev 72:153–178

    Article  Google Scholar 

  • Jonsson M, Allahgholi L, Sardari RRR, Hreggviosson GO, Karlsson EN (2020) Extraction and modification of macroalgal polysaccharides for current and next-generation applications. Molecules 25:930

    Article  PubMed Central  CAS  Google Scholar 

  • Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, Buxton S, Cooper A, Markowitz S, Duran C, Thierer T (2012) Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28:1647–1649

    Article  PubMed  PubMed Central  Google Scholar 

  • Khan SA, Kumar S, Hussain MZ, Kalra N (2009) Climate change, climate variability and Indian agriculture: impacts vulnerability and adaptation strategies. In: Singh SN (ed) Climate change and crops. Springer, Berlin, pp 19–38

    Chapter  Google Scholar 

  • Kittinger JN, Bambico TM, Minton D, Miller A, Mejia M, Kalei N, Wong B, Glazier EW (2016) Restoring ecosystems, restoring community: socioeconomic and cultural dimensions of a community-based coral reef restoration project. Reg Environ Chang 16:301–313

    Article  Google Scholar 

  • Klindworth A, Pruesse E, Schweer T, Peplies J, Quast C, Horn M, Glöckner FO (2013) Evaluation of general 16S ribosomal RNA gene PCR primers for classical and next-generation sequencing-based diversity studies. Nucleic Acids Res 41:e1–e1

    Article  CAS  PubMed  Google Scholar 

  • Kozich JJ, Westcott SL, Baxter NT, Highlander SK, Schloss PD (2013) Development of a dual-index sequencing strategy and curation pipeline for analyzing amplicon sequence data on the MiSeq Illumina sequencing platform. Appl Environ Microbiol 79:5112–5120

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kraan S (2012) Algal polysaccharides, novel applications and outlook. In: Chang C-F (ed) Carbohydrates-comprehensive studies on glycobiology and glycotechnology. IntechOpen, Riejeka

    Google Scholar 

  • López-Mondéjar R, Zhlke D, Becher D, Reidel K, Baldrian P (2016) Cellulose and hemicellulose decomposition by forest soil bacteria proceeds by the action of structurally variable enzymatic systems. Sci Rep 6:25279

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lourenço SO, Barbarino E, De-Paula JC, Pereira LODS, Marquez UML (2002) Amino acid composition, protein content and calculation of nitrogen-to-protein conversion factors for 19 tropical seaweeds. Phycol Res 50:233–241

    Article  Google Scholar 

  • Mäkelä MR, Marinović M, Nousiainen P, Liwanag AJ, Benoit I, Sipilä J, Hatakka A, de Vries RP, Hilden KS (2015) Aromatic metabolism of filamentous fungi in relation to the presence of aromatic compounds in plant biomass. Adv Appl Microbiol 91:63–137

    Article  PubMed  CAS  Google Scholar 

  • Martinez JA, Smith CM, Richmond RH (2012) Invasive algal mats degrade coral reef physical habitat quality. Estuar Coast Shelf Sci 99:42–49

    Article  CAS  Google Scholar 

  • McMurtry GM, Wiltshire JC, Kauahikaua JP (1995) Heavy metal abnormalities in coastal sediments of O’ahu, Hawai’i’. Pac Sci 49:452–470

    CAS  Google Scholar 

  • Michalak I, Tuhy Ł, Saeid A, Chojnacka K (2013) Bioavailability of Zn (II) to plants from new fertilizer components produced by biosorption. Inter J Agron Plant Prod 4:3522–3536

    CAS  Google Scholar 

  • Michalak I, Wilk R, Chojnacka K (2017) Bioconversion of Baltic seaweeds into organic compost. Waste Biomass Valoriz 8:1885–1895

    Article  CAS  Google Scholar 

  • Myklestae S (1964) Experiments with seaweed as a supplemental fertilizer. Proc Int Seaweed Symp 4:432–438

    Google Scholar 

  • Ortiz-Matamoros MF, Villanueva MA, Islas-Flores T (2018) Genetic transformation of cell-walled plant and algae cells: delivering DNA through the cell wall. Brief Funct Genom 17:26–33

    Article  CAS  Google Scholar 

  • Popper ZA, Michel G, Hervé C, Domozych DS, Willats WG, Tuohy MG, Kloareg B, Stengel DB (2011) Evolution and diversity of plant cell walls: from algae to flowering plants. Annu Rev Plant Biol 62:567–590

    Article  CAS  PubMed  Google Scholar 

  • Prakash A, Thavaselvam D, Kumar A, Kumar A, Arora S, Tiwari S, Barua A, Sathyaseelan K (2014) Isolation, identification and characterization of Burkholderia pseudomallei from soil of coastal region of India. Springerplus 3:438

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Radovich TJK, Pant A, Gurr I, Hue N, Sugano J, Sipes B, Arancon N, Tamaru C, Fox BK, Kobayashi B (2012) Innovative use of locally produced inputs to improve plant growth, crop quality, and grower profitability in Hawai’i’. HortTechnology 22:738–742

    Article  Google Scholar 

  • Reppun FAWL (2016) Invasive marine algae as a soil amendment for island farmers: agronomic and ethonogrpahic assessment of implications for nutrient management. Graduate Program in Environmental Science, Ohio State University

  • Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, Sahl JW (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sharifuzzaman SM, Rahman H, Ashekuzzaman SM, Islam MM, Chowdhury SR, Hossain MS (2016) Heavy metals accumulation in coastal sediments. In: Hasegawa H, Rahman I, Rahman M (eds) Environmental Remediation Technologies for Metal-Contaminated Soils. Springer, Tokyo, pp 21–42

    Chapter  Google Scholar 

  • Siegwald L, Touzet H, Lemoine Y, Hot D, Audebert C, Caboche S (2017) Assessment of common and emerging bioinformatics pipelines for targeted metagenomics. PLoS One 12:e0169563

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Simberloff D (2012) Sustainability of biodiversity under global changes, with particular reference to biological invasions. In: Weinstein MP, Turner E (eds) Sustainability Science. Springer, New York, pp 139–157

    Chapter  Google Scholar 

  • Smith JE, Hunter CL, Smith CM (2002) Distribution and reproductive characteristics of nonindigenous and invasive marine algae in the Hawaiian Islands. Pac Sci 56:299–325

    Article  Google Scholar 

  • Stiger-Pouvreau V, Bourgougnon N, Deslandes E (2016) Carbohydrates from Seaweeds. In: Fleurence J, Levine I (eds) Seaweed in Health and Disease Prevention. Academic Press, Amsterdam, pp 223–274

  • Strain EM, Thomson RJ, Micheli F, Mancuso FP, Airoldi L (2014) Identifying the interacting roles of stressors in driving the global loss of canopy-forming to mat-forming algae in marine ecosystems. Glob Chang Biol 20:3300–3312

    Article  PubMed  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

    Article  CAS  PubMed  Google Scholar 

  • USDA (2000) Heavy metal soil contamination’. https://www.nrcs.usda.gov/Internet/FSE_DOCUMENTS/nrcs142p2_053279.pdf

  • Viola R, Nyall P, Pedersen M (2001) The unique features of starch metabolism in red algae. Proc Biol Sci 268:1417–1422

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang D, Li C, Parikh SJ, Scow KM (2019) Impact of biochar on water retention of two agricultural soils–a multi-scale analysis. Geoderma 340:185–191

    Article  CAS  Google Scholar 

  • Weijerman M, Most R, Wong K, Beavers S (2008) Attempt to control the invasive red alga Acanthophora spicifera (Rhodophyta: Ceramiales) in a Hawaiian fishpond: an assessment of removal techniques and management options. Pac Sci 62:517–532

  • Westbrook CE, Ringang RR, Cantero SMA, Toonen RJ (2015) Survivorship and feeding preferences among size classes of outplanted sea urchins, Tripneustes gratilla, and possible use as biocontrol for invasive alien algae. Peer J 3:e1235

    Article  PubMed  PubMed Central  Google Scholar 

  • Wuana RA, Okieimen FE (2011) Heavy metals in contaminated soils: a review of sources, chemistry, risks, and best available strategies for remediation. ISRN Ecology 2011:402647

  • Xu SY, Huang X, Cheong KL (2017) Recent advances in marine algae polysaccharides: isolation, structure and activities. Mar Drugs 15:388

    Article  PubMed Central  CAS  Google Scholar 

  • Yu SK, Blennow A, Bojko M, Madsen F, Olsen CE, Engelsen SB (2002) Physico-chemical characterization of floridean starch of red algae. Starch-Starke 54:66–74

    Article  CAS  Google Scholar 

  • Yuvaraj D, Gayarthri PK (2017) Impact of seaweeds in agriculture. In: Nabti E (ed) Biotechnological application of seaweeds. Nova Scientific Publishers, New York, pp 25–46

    Google Scholar 

  • Zheng LX, Chen XQ, Cheong KL (2020) Current trends in marine algae polysaccharides: the digestive tract, microbial catabolism, and prebiotic potential. Int J Biol Macromol 151:344–354

    Article  CAS  PubMed  Google Scholar 

  • Zodape ST (2001) Seaweeds as a biofertilizer. J Sci Ind Res 60:378–382

    Google Scholar 

  • ΜcGuire KL, Treseder KK (2010) Microbial communities and their relevance for ecosystem models: decomposition as a case study. Soil Biol Biochem 42:529–535

    Article  CAS  Google Scholar 

  • Macduff SD (2018) Enhancing coral reef resilience and restoration success: lessons learned from Laolao bay, Saipan and Maunalua bay, Oahu. Ph.D disseratation University of Hawaii. pp 27 https://scholarspace.manoa.hawaii.edu/bitstream/10125/62842/2018-08-phd-macduff.pdf. Accessed 6 Oct 2019

Download references

Funding

This work was supported in part by grants N00014-17-1-2206 from the US Office of Naval Research, the Oiwi Undergraduate Research Fellowship (OURF), and the Native Hawaiian Science and Engineering Mentorship Program (NHSEMP).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to B. Yoza.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Sabate, K., Masutani, S. & Yoza, B. Microbiological degradation of macroalgae waste and its potential considerations for agricultural applications. J Appl Phycol 33, 2645–2654 (2021). https://doi.org/10.1007/s10811-021-02480-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10811-021-02480-6

Keywords

Navigation