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.
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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
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
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
Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410
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
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
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
Battacharyya D, Babgohari MZ, Rathor P, Prithiviraj B (2015) Seaweed extracts as biostimulants in horticulture. Sci Hort 196:39–48
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
Bo S, Lortscher P, Palfery D (2013) Algal biomass anaerobic biodegradability. J Appl Phycol 25:757–761
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
Bugg TD, Ahmad M, Hardiman EM, Rahmanpour R (2011) Pathways for degradation of lignin in bacteria and fungi. Nat Prod Rep 28:1883–1896
Chapman RL (2013) Algae: the world’s most important “plants”—an introduction. Mitig Adapt Strat Global Change 18:5–12
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
Cole AJ, Roberts DA, Garside AL, de Nys R, Paul NA (2016) Seaweed compost for agricultural crop production. J Appl Phycol 28:629–642
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
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
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
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
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
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
Gacesa P (1992) Enzymatic degradation of alginates. Int J Biochem 24:545–552
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
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
Han W, Clarke W, Pratt S (2014) Composting of waste algae: a review. Waste Manag 34:1148–1155
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
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
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
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
Inderjit, Chapman D, Ranelletti M, Kaushik S (2006) Invasive marine algae: an ecological perspective. Bot Rev 72:153–178
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
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
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
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
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
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
Kraan S (2012) Algal polysaccharides, novel applications and outlook. In: Chang C-F (ed) Carbohydrates-comprehensive studies on glycobiology and glycotechnology. IntechOpen, Riejeka
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
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
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
Martinez JA, Smith CM, Richmond RH (2012) Invasive algal mats degrade coral reef physical habitat quality. Estuar Coast Shelf Sci 99:42–49
McMurtry GM, Wiltshire JC, Kauahikaua JP (1995) Heavy metal abnormalities in coastal sediments of O’ahu, Hawai’i’. Pac Sci 49:452–470
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
Michalak I, Wilk R, Chojnacka K (2017) Bioconversion of Baltic seaweeds into organic compost. Waste Biomass Valoriz 8:1885–1895
Myklestae S (1964) Experiments with seaweed as a supplemental fertilizer. Proc Int Seaweed Symp 4:432–438
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
Zodape ST (2001) Seaweeds as a biofertilizer. J Sci Ind Res 60:378–382
ΜcGuire KL, Treseder KK (2010) Microbial communities and their relevance for ecosystem models: decomposition as a case study. Soil Biol Biochem 42:529–535
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
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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).
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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
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DOI: https://doi.org/10.1007/s10811-021-02480-6