Skip to main content
SpringerLink
Log in

The role of fungi in processing marine organic matter in the upwelling ecosystem off Chile

  • Original Paper
  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

In a study that spanned from March 2007 through November 2009, we report high fungal biomass and over 90% of extracellular enzymatic activity occurring in the size classes dominated by fungi during periods of high autotrophic biomass in surface waters of the upwelling ecosystem off central-southern Chile (36°30.80′S–73°07.70′W). Fungal biomass in the water column was determined by the abundance of hyphae and was positively correlated with the concentration of the fungal biomarker 18:2ω6. High fungal biomass during active upwelling periods was comparable to that of prokaryotes (bacteria plus archaea) and was associated with an increase in phytoplankton biomass and in extracellular enzymatic hydrolysis in waters from the depth of maximum fluorescence. We show fungi as a new microbial component in the coastal upwelling ecosystem of the Humboldt Current System off central Chile. Our results suggest that the temporal pattern in fungal biomass in the water column during a year cycle is a reflection of their capacity to hydrolyze organic polymers and, in consequence, fungal biomass and activity respond to a seasonal cycle of upwelling in this ecosystem.

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.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

References

  • Amon RMW, Benner R (1994) Rapid cycling of high-molecular-weight dissolved organic matter in the ocean. Nature 369:549–552

    Article  CAS  Google Scholar 

  • Anabalón V, Morales CE, Escribano R, Varas MA (2007) The contribution of nano- and micro-planktonic assemblages in the surface layer (0–30 m) under different hydrographic conditions in the upwelling area off Concepción, central Chile. Prog Oceanogr 75:396–414

    Article  Google Scholar 

  • Anderson TF (1951) Techniques for preservation of the three-dimensional structure in preparing specimens for the electron microscope. Trans NY Acad Sci 13:130–134

    Google Scholar 

  • Arnosti C (2003) Microbial extracellular enzymes and their role in DOM cycling. In: Findley S, Sinsabaugh RS (eds) Aquatic ecosystems: interactivity of dissolved organic matter. Academic Press, USA, pp 315–342

    Google Scholar 

  • Azam F, Hodson RE (1977) Size distribution and activity of marine microheterotrophs. Limnol Oceanogr 22:492–501

    Article  CAS  Google Scholar 

  • Balkwill DL, Leach FR, Wilson JT, McNabb JF, White DC (1988) Equivalence of microbial biomass measures based on membrane lipid and cell wall components, adenosinetriphosphate, and direct counts in subsurface aquifer sediments. Microbial Ecol 16:73–84

    Article  CAS  Google Scholar 

  • Benner R, Pakulski JD, McCarthy M, Hedges JI, Hatcher PG (1992) Bulk chemical characterization of dissolved organic matter in the ocean. Science 255:1561–1564

    Article  CAS  Google Scholar 

  • Biddanda B, Benner R (1997) Carbon, nitrogen, and carbohydrate fluxes during the production of particulate and dissolved organic matter by marine phytoplankton. Limnol Oceanogr 42:506–518

    Article  CAS  Google Scholar 

  • Biersmith A, Benner R (1998) Carbohydrates in phytoplankton and freshly produced dissolved organic matter. Mar Chem 63:133–144

    Article  Google Scholar 

  • Bligh EG, Dyer WJ (1959) A rapid method for total lipid extraction and purification. Can J Biochem Physiol 37:911–917

    CAS  Google Scholar 

  • Boschker HTS, Middelburg JJ (2002) Stable isotopes and biomarkers in microbial ecology. FEMS Microbiol Ecol 40:85–95

    Article  CAS  Google Scholar 

  • Buchalo AS, Nevo E, Wasser SP, Volz PA (2000) Newly discovered halophilic fungi in the Dead Sea (Israel). In: Seckbach J (ed) Journey to diverse microbial worlds. Kluwer, Dordrecht, The Netherlands, pp 239–252

    Google Scholar 

  • Carlile MJ, Watkinson SC, Gooday GW (2001) The fungi, 2nd edn. Academic Press, San Diego

    Google Scholar 

  • Carlson CA (2002) Production and removal processes. In: Hansell DA, Carlson CA (eds) Biogeochemistry of marine dissolved organic matter. Elsevier Science, San Diego, pp 91–151

    Chapter  Google Scholar 

  • Chavez FP, Buck KR, Coale KH, Martin JH, DiTullio GR, Welschmeyer NA, Jacobson AC, Barber RT (1991) Growth rates, grazing, sinking, and iron limitation of equatorial Pacific phytoplankton. Limnol Oceanogr 36:1816–1833

    Article  CAS  Google Scholar 

  • Christie WW (1989) The preparation of derivatives of fatty acids. In: Christie WW (ed) Gas chromatography and lipids: a practical guide. The Oily Press, Ltd., Ayr, Scotland, pp 36–39

    Google Scholar 

  • Christie WW (1998) Gas chromatography-mass spectrometry methods for structural analysis of fatty acids. Lipids 33:343–353

    Article  CAS  Google Scholar 

  • Chróst RJ (1991) Environmental control of the synthesis and activity of aquatic microbial ectoenzymes. In: Chróst RJ (ed) Microbial enzymes in aquatic environments. Springer, New York, pp 29–59

    Google Scholar 

  • Chróst RJ, Riemann B (1994) Storm-stimulated enzymatic decomposition of organic matter in benthiclpelagic coastal mesocosms. Mar Ecol Prog Ser 108:185–192

    Article  Google Scholar 

  • Clipson N, Otte M, Landy E (2006) Biogeochemical roles of fungi in the marine and estuarine habitats. In: Gadd GM (ed) Fungi in biogeochemical cycles. Cambridge university press, New York, pp 436–461

    Chapter  Google Scholar 

  • Cooney JJ, Doolittle MM, Grahl-Nielsen O, Haaland IM, Kirk PW Jr (1993) Comparison of fatty acids of marine fungi using multivariate statistical analysis. J Ind Microbiol 12:373–378

    Article  CAS  Google Scholar 

  • Crumb BC, Baros JA, Simenstad CA (1998) Dominance of particle-attached bacteria in the Columbia River estuary, USA. Aquat Microb Ecol 14:7–18

    Article  Google Scholar 

  • Cuevas LA, Daneri G, Jacob B, Montero P (2004) Microbial abundance and activity in the seasonal upwelling area off Concepción (36°S), central Chile: a comparison of upwelling and non-upwelling conditions. Deep-Sea Res Pt II 51:2427–2440

    Article  CAS  Google Scholar 

  • Damare S, Raghukumar C (2008) Fungi and macroaggregation in deep-sea sediments. Microb Ecol 56:168–177

    Article  Google Scholar 

  • Damare S, Raghukumar C, Raghukumar S (2006) Fungi in deep-sea sediments of the Central Indian Basin. Deep-Sea Res Pt I 53:14–27

    Article  Google Scholar 

  • Daneri G, Dellarossa V, Quiñones R, Jacob B, Montero P, Ulloa O (2000) Primary production and community respiration in the Humboldt current system off Chile and associated oceanic areas. Mar Ecol Prog Ser 197:41–49

    Article  Google Scholar 

  • Das S, Lyla PS, Khan SA (2007) Fatty acid profiles of marine benthic microorganisms isolated from the continental slope of Bay of Bengal: a possible implications in the benthic food web. Ocean Sci J 42:247–254

    Article  CAS  Google Scholar 

  • Devi P, Shridar MPD, D’Souza L, Naik CG (2006) Cellular composition of marine-derived fungi. Ind J Mar Sci 35:359–363

    CAS  Google Scholar 

  • Dighton J (2007) Nutrient cycling by saprotrophic fungi in terrestrial habitats. In: Kubicek CP, Druzhinina IS (eds) The Mycota IV, environmental and microbial relationships, 2nd edn. Springer, Berlin, pp 287–300

    Google Scholar 

  • Eppley RW, Chavez FP, Barber RT (1992) Standing stocks of particulate carbon and nitrogen in the equatorial Pacific at 150°W. J Geophys Res 97:655–661

    Article  Google Scholar 

  • Fell JW, Newell SY (1998) Biochemical and molecular methods for the study of marine fungi. In: Cooksey KE (ed) Biochemical and molecular methods for the study of marine fungi. Chapman and Hall, London, pp 259–283

    Google Scholar 

  • Figueroa AD, Moffat C (2000) On the influence of topography in the induction of coastal upwelling along the Chilean coast. Geophys Res Lett 27:3905–3908

    Article  Google Scholar 

  • Frostegard A, Baath E (1996) The use of phospholipids fatty acids analysis to estimate bacterial and fungal biomass in soil. Biol Fertil Soil 22:59–65

    Article  Google Scholar 

  • Gessner MO, Gulis V, Kuehn KA, Chauvet E, Suberkropp K (2007) Fungal decomposers of plant litter in aquatic ecosystems. In: Kubicek CP, Druzhinina IS (eds) The Mycota IV, environmental and microbial relationships, 2nd edn. Springer, Berlin, pp 301–324

    Google Scholar 

  • González HE, Daneri G, Figueroa D, Iriarte L, Lefevre N, Pizarro G, Quiñones RA, Sobarzo M, Troncoso A (1998) Producción primaria y su destino en la trama trófica pelágica y océano profundo e intercambio océano-atmósfera de CO2 en la zona norte de la corriente de Humboldt (23°S): posibles efectos del evento El Niño 1997–1998. Rev Chil Hist Nat 71:429–458

    Google Scholar 

  • Gulis V, Kuehn K, Suberkropp K (2006) The role of fungi in carbon and nitrogen cycles in freshwater ecosystems. In: Gadd GM (ed) Fungi in biogeochemical cycles. Cambridge University Press, New York, pp 405–435

    Google Scholar 

  • Hedges JI (1992) Global geochemical cycles: progress and problems. Mar Chem 39:67–93

    Article  CAS  Google Scholar 

  • Hoppe H-G (1983) Significance of exoenzymatic activities in the ecology of brackish water: measurements by means of methylumbelliferyl-substrates. Mar Ecol Prog Ser 11:299–308

    Article  CAS  Google Scholar 

  • Hoppe HG, Kim S-J, Gocke K (1988) Microbial decomposition in aquatic environments: a combined process of extracellular enzyme activity and substrate uptake. Appl Environ Microbiol 54:784–790

    CAS  Google Scholar 

  • Hoppe HG, Arnosti C, Herndel GF (2002) Ecological significance of bacterial enzymes in marine environment. In: Burns RC, Dick RP (eds) Microbial enzymes in the environment activity, ecology, and applications. Marcel Dekker, Inc, New York, pp 73–107

    Google Scholar 

  • Hyde K, Jones EBG, Leaño E, Pointing S, Poonyth AD, Vrijmoed L (1998) Role of fungi in marine ecosystem. Biodivers Conserv 7:1147–1161

    Article  Google Scholar 

  • Jebaraj CS, Raghukumar C (2009) Anaerobic denitrification in fungi from the coastal marine sediments off Goa, India. Mycol Res 113:100–109

    Article  Google Scholar 

  • Jorgensen NOG, Kroer N, Coffin RB, Hoch MP (1999) Relations between bacterial nitrogen metabolism and growth efficiency in an estuarine and an open-water ecosystem. Aquat Microb Ecol 18:247–261

    Article  Google Scholar 

  • Karner M, Fuks D, Herndl GJ (1992) Bacterial activity along a trophic gradient. Microb Ecol 24:243–257

    Article  Google Scholar 

  • Kaur A, Chaudhary A, Kaur A, Choudhary R, Kaushik R (2005) Phospholipid fatty acid—a bioindicator of environment monitoring and assessment in soil ecosystem. Curr Sci India 89:1103–1112

    CAS  Google Scholar 

  • Kiersztyn B, Siuda W, Chróst RJ (2002) Microbial ectoenzyme activity: useful parameters for characterizing the trophic conditions of lakes. Pol J Environ Stud 11:367–373

    CAS  Google Scholar 

  • Kis-Papo T, Oren A, Wasser SP, Nevo E (2003) Survival of filamentous fungi in hypersaline Dead Sea water. Microbial ecol 45:183–190

    Article  CAS  Google Scholar 

  • Lai X, Cao L, Tan H, Fang S, Huang Y, Zhou S (2007) Fungal communities from methane hydrate-bearing deep-sea marine sediments in South China Sea. ISME J 1:756–762

    Article  CAS  Google Scholar 

  • Lalli CM, Parsons TR (1996) Biological oceanography: an introduction. Butterworth/Heinemann, Oxford

    Google Scholar 

  • Le Calvez T, Burgaud G, Mahé S, Barbier G, Vandenkoornhuyse P (2009) Fungal diversity in deep-sea hydrothermal ecosystem. Appl Environ Microbiol 75:6415–6421

    Article  Google Scholar 

  • Lindahl BD, de Boer W, Finlay RD (2010) Disruption of root carbon transport into forest humus stimulates fungal opportunists at the expense of mycorrhizal fungi. ISME J 4:872–881

    Article  Google Scholar 

  • Magan N (2007) Fungi in extreme environments. In: Kubicek CP, Druzhinina IS (eds) The Mycota IV, environmental and microbial relationships, 2nd edn. Springer, Berlin, pp 85–103

    Google Scholar 

  • Méjanelle L, Laureillard J (2008) Lipid biomarker record in surface sediments at three sites of contrasting productivity in the tropical North Eastern Atlantic. Mar Chem 108:59–76

    Article  Google Scholar 

  • Meyer-Reil L-A (1987) Seasonal and spatial distribution of extracellular enzymatic activities and microbial incorporation of dissolved organic substrates in marine sediments. Appl Environ Microbiol 53:1748–1755

    CAS  Google Scholar 

  • Misic C, Castellano M, Fabiano M, Ruggirei N, Saggiamo V, Povero P (2006) Ectoenzymatic activity in surface waters: a transect from the Mediterranean Sea across the Indian Ocean to Australia. Deep-Sea Res Pt I 53:1517–1532

    Article  CAS  Google Scholar 

  • Montero P, Daneri G, Cuevas LA, González HE, Jacob B, Lizárraga L, Menschel E (2007) Productivity cycles in the coastal upwelling area off Concepción: the importance of diatoms and bacterioplankton in the organic carbon flux. Prog Oceanog 75:518–530

    Article  Google Scholar 

  • Naush M, Pollenhe F, Kerstan E (1998) Extracellular enzyme activities in relation to hydrodynamics in the Pomeranian Bight (Southern Baltic Sea). Microb Ecol 36:251–258

    Article  Google Scholar 

  • Nichols DS, Nichols PD, Sullivan CW (1993) Fatty acid, sterol and hydrocarbon composition of Antarctic sea ice diatom communities during the spring bloom in McMurdo Sound. Antarc Sci 5:271–278

    Google Scholar 

  • Olsson PA (1999) Signature fatty acids provide tools for determination of the distribution and interactions of mycorrhizal fungi in soil. FEMS Microbiol Ecol 29:303–310

    Article  CAS  Google Scholar 

  • Pantoja S, Lee C (1994) Cell-surface oxidation of amino acids in seawater. Limnol Oceanogr 39:1718–1726

    Article  CAS  Google Scholar 

  • Pantoja S, Rossel P, Castro R, Cuevas LA, Daneri G, Córdova C (2009) Microbial degradation rates of small peptides and amino acids in the oxygen minimum zone of Chilean coastal waters. Deep-Sea Res Pt II 56:1055–1062

    Article  CAS  Google Scholar 

  • Parsons T, Maita Y, Lalli C (1984) A manual of chemical and biological method for seawater analysis. Pergamon Press, Great Britain

    Google Scholar 

  • Porter KG, Feig YS (1980) The use of DAPI for identifying and counting aquatic microflora. Limnol Oceanogr 25:943–948

    Article  Google Scholar 

  • Raghukumar S (2005) The role of fungi in marine detrital processes. In: Ramaiah N (ed) Marine microbiology: facets & opportunities. National Institute of Oceanography, Goa, India, pp 91–101

    Google Scholar 

  • Rasconi S, Jobard M, Jouve L, Sime-Ngando T (2009) Use of calcofluor white for detection, identification, and quantification of phytoplanktonic fungal parasites. Appl Environ Microbiol 75:2545–2553

    Article  CAS  Google Scholar 

  • Rath J, Schiller C, Herndl GJ (1993) Ectoenzymatic activity and bacterial dynamics along a trophic gradient in the Caribbean Sea. Mar Ecol Prog Ser 102:89–96

    Article  CAS  Google Scholar 

  • Riemann L, Steward FG, Azam F (2000) Dynamics of bacterial community composition and activity during a mesocosm diatom bloom. Appl Environ Microbiol 66:578–587

    Article  CAS  Google Scholar 

  • Rosso AL, Azam F (1987) Proteolytic activity in coastal oceanic waters: depth distribution and relationship to bacterial populations. Mar Ecol Prog Ser 41:231–241

    Article  CAS  Google Scholar 

  • Smith DC, Steward GF, Long RA, Azam F (1995) Bacterial mediation of carbon fluxes during a diatom bloom in a mesocosm. Deep-Sea Res Pt II 42:75–97

    Article  CAS  Google Scholar 

  • Sobarzo M, Bravo L, Donoso D, Garcés-Vargas J, Schneider W (2007) Coastal upwelling and seasonal cycles that influence the water column over the continental shelf off central Chile. Prog Oceanogr 75:363–382

    Article  Google Scholar 

  • Strom SL, Benner R, Ziegler S, Dagg MJ (1997) Planktonic grazers are a potentially important source of marine dissolved organic carbon. Limnol Oceanogr 42:1364–1374

    Article  CAS  Google Scholar 

  • Strub PT, Mesias J, Montecino V, Rutllant J, Salinas S (1998) Coastal ocean circulation off western South America, Coastal Segment (6, E). In: Robinson A, Brink K (eds) The Sea, vol 11. Wiley, New York, pp 273–313

    Google Scholar 

  • Tolosa I, Vescovali I, Leblond N, Marty JC, De Mora S, Prieur L (2004) Distribution of pigments and fatty acids biomarkers in particulate matter from the frontal structure of the Alboran Sea (SW Mediterranean Sea). Mar Chem 88:103–125

    Article  CAS  Google Scholar 

  • Troncoso VA, Daneri G, Cuevas LA, Jacob B, Montero P (2003) Bacterial carbon flow in the Humboldt current system off Chile. Mar Ecol Prog Ser 250:1–12

    Article  CAS  Google Scholar 

  • Unanue M, Azúa I, Barcina I, Egea L, Iriberri J (1993) Size distribution of aminopeptidase activity and bacterial incorporation of dissolved substrates in three aquatic ecosystems. FEMS Microbiol Lett 102:175–183

    Article  CAS  Google Scholar 

  • van Veen JA, Paul EA (1979) Conversion of biovolume measurements of soil organisms, grown under various moisture tensions, to biomass and their nutrient content. Appl Environ Microbiol 37:686–692

    Google Scholar 

  • Vargas CA, Martínez RA, Cuevas LA, Pavez MA, Cartes C, González HE, Escribano RE, Daneri G (2007) The relative importance of microbial and classical food webs in a highly productive coastal upwelling area. Limnol Oceanogr 52:1495–1510

    Google Scholar 

  • Vestal JR, White DC (1989) Lipid analysis in microbial ecology quantitative approaches to the study of microbial communities. Bioscience 39:535–541

    Article  CAS  Google Scholar 

  • White DC, Davis WM, Nickels JS, King JD, Bobie RJ (1979) Determination of the sedimentary microbial biomass by extractable lipid phosphate. Oecologia 40:51–62

    Article  Google Scholar 

  • Zhukova NV, Aizdaicher NA (1995) Fatty acid composition of 15 species of marine microalgae. Phytochemistry 39:351–356

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This research was funded by the Programa de Investigación Marina de Excelencia, PIMEX-Nueva Aldea (University of Concepcion and Celulosa Arauco y Constitución S.A.) and the COPAS Center (Grant 150100007, CONICYT, Chile). We are thankful to the COPAS Time Series team and the R/V Kay-Kay II crew for their valuable help during field work. We also wish to thank Lilian Nuñez, Rodrigo Castro, Jaime Soto and Patricio Ampuero from the Marine Organic Geochemistry laboratory at UDEC for their valuable help in the laboratory analyses. MG acknowledges the support of the Agreement Fundación Andes/Wood Hole Oceanographic Institution/University of Concepción for funding his research visit to the laboratory of Professor Jack Fell at University of Miami.

Author information

Authors and Affiliations

  1. Graduate Program in Oceanography, Department of Oceanography, University of Concepcion, P. O. Box 160-C, Concepcion, Chile

    M. H. Gutiérrez

  2. Department of Oceanography and Center for Oceanographic Research in the Eastern South Pacific, University of Concepcion, P. O. Box 160-C, Concepcion, Chile

    S. Pantoja & R. A. Quiñones

  3. Program of Marine Research of Excellence (PIMEX-Nueva Aldea), Faculty of Natural and Oceanographic Sciences, University of Concepcion, P. O. Box 160-C, Concepcion, Chile

    M. H. Gutiérrez, S. Pantoja, E. Tejos & R. A. Quiñones

Authors
  1. M. H. Gutiérrez
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. S. Pantoja
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. E. Tejos
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. R. A. Quiñones
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to S. Pantoja.

Additional information

Communicated by M. Huettel.

Electronic supplementary material

Below is the link to the electronic supplementary material.

(PDF 5889 kb)

(PDF 69 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Gutiérrez, M.H., Pantoja, S., Tejos, E. et al. The role of fungi in processing marine organic matter in the upwelling ecosystem off Chile. Mar Biol 158, 205–219 (2011). https://doi.org/10.1007/s00227-010-1552-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00227-010-1552-z

Keywords

Search

Navigation