Skip to main content
SpringerLink
Log in

Interplay between proteases and protease inhibitors in the sea fan—Aspergillus pathosystem

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

Abstract

Environmental conditions greatly impact the dynamics of host–pathogen relationships, affecting outbreaks and emergence of new diseases. In corals, epizootics have been a main contributor to the decline of reef ecosystems and rising sea surface temperatures associated with climate change are thought to exacerbate virulence of pathogens and/or compromise the immune responses of coral hosts. Among pathogens strategies, protease secretion is a common virulence factor that promotes colonization of the host. As such, protease inhibitors play an invaluable role to the host for protection against pathogen invasion. This study describes changes in activity of proteases secreted by the fungal pathogen, Aspergillus sydowii, and protease inhibitors of Gorgonia ventalina under ambient and elevated temperatures and health conditions (disease and healthy). G. ventalina colonies were collected from Florida Keys, Florida (24° 34.138N, 81° 22.905W) or La Parguera, Puerto Rico (17° 56.091N, 67° 02.577W) in 2007 and 2012, respectively. At elevated temperatures, protease activity was significantly higher than at ambient temperatures in A. sydowii. Temperature stress did not induce a change in protease inhibitor activity, but in healthy G. ventalina colonies, inhibitor activity against proteases was higher than in diseased individuals. Healthy colonies appear capable of resisting proteolytic activity, but diseased individuals are still likely affected by pathogen infections. These data suggest that rising sea surface temperatures due to climate change may increase levels of virulence (protease activity) of A. sydowii, while immunity (protease inhibitor) of G. ventalina may not be affected.

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

Similar content being viewed by others

References

  • Alker AP, Smith GW, Kim K (2001) Characterization of Aspergillus sydowii (Thom et Church), a fungal pathogen of Caribbean sea fan corals. Hydrobiologia 460:105–111

    Article  Google Scholar 

  • Altizer S, Ostfeld RS, Johnson PTJ, Kutz S, Harvell CD (2013) Climate change and infectious diseases: from evidence to a predictive framework. Science 341:514–519. doi:10.1126/science.1239401

    Article  CAS  Google Scholar 

  • Armstrong PB (2006) Proteases and protease inhibitors: a balance of activities in host–pathogen interaction. Immunobiology 211:263–281

    Article  CAS  Google Scholar 

  • Asis R, Muller V, Barrionuevo DL, Araujo SA, Aldao MA (2009) Analysis of protease activity in Aspergillus flavus and A. parasiticus on peanut seed infection and aflatoxin contamination. Eur J Plant Pathol 124:391–403. doi:10.1007/s10658-008-9426-7

    Article  CAS  Google Scholar 

  • Bond JS, Butler PE (1987) Intracellular proteases. Annu Rev Biochem 56:333–364. doi:10.1146/annurev.bi.56.070187.002001

    Article  CAS  Google Scholar 

  • Bruno JF, Ellner SP, Vu I, Kim K, Harvell CD (2011) Impacts of aspergillosis on sea fan coral demography: modeling a moving target. Ecol Monogr 81:123–139

    Article  Google Scholar 

  • Burge CA, Mouchka ME, Harvell CD, Roberts S (2013) Immune response of the Caribbean sea fan, Gorgonia ventalina, exposed to an Aplanochytrium parasite as revealed by transcriptome sequencing. Front Physiol 4

  • Cerenius L, Soderhall K (2004) The prophenoloxidase-activating system in invertebrates. Immunol Rev 198:116–126

    Article  CAS  Google Scholar 

  • Cohen BL (1973) Regulation of intracellular and extracellular neutral and alkaline proteases in Aspergillus nidulans. J Gen Microbiol 79:311–320. doi:10.1099/00221287-79-2-311

    Article  CAS  Google Scholar 

  • Donpudsa S, Tassanakajon A, Rimphanitchayakit V (2009) Domain inhibitory and bacteriostatic activities of the five-domain Kazal-type serine proteinase inhibitor from black tiger shrimp Penaeus monodon. Dev Comp Immunol 33:481–488

    Article  CAS  Google Scholar 

  • Dunaevskii YE, Gruban TN, Belyakova GA, Belozerskii MA (2006) Extracellular proteinases of filamentous fungi as potential markers of phytopathogenesis. Microbiology 75:649–652. doi:10.1134/S0026261706060051

    Article  CAS  Google Scholar 

  • Faisal M, MacIntyre E, Adham K, Tall B, Kothary M, La Peyre J (1998) Evidence for the presence of protease inhibitors in eastern (Crassostrea virginica) and Pacific (Crassostrea gigas) oysters. Comp Biochem Physiol B 121:161–168

    Article  Google Scholar 

  • Flynn K, Weil E (2009) Variability of aspergillosis in Gorgonia ventalina in La Parguera, Puerto Rico. Caribb J Sci 45:215–220

    Google Scholar 

  • Geiser DM, Taylor JW, Ritchie KB, Smith GW (1998) Cause of sea fan death in the West Indies. Nature 394:137–138

    Article  CAS  Google Scholar 

  • Gil-Agudelo DL, Myers C, Smith GW, Kim K (2006) Changes in the microbial communities associated with Gorgonia ventalina during aspergillosis infection. Dis Aquat Org 69:89

    Article  Google Scholar 

  • Gil-Turnes M, Hay M, Fenical W (1989) Symbiotic marine bacteria chemically defend crustacean embryos from a pathogenic fungus. Science 246:116–118. doi:10.1126/science.2781297

    Article  CAS  Google Scholar 

  • Hanzi M, Shimizu M, Hearn VM, Monod M (1993) A study of the alkaline proteases secreted by different Aspergillus species. Mycoses 36:351–356

    Article  CAS  Google Scholar 

  • Harvell D (2004) Ecology and evolution of host-pathogen interactions in nature. Am Nat 164:S1–S5

    Article  Google Scholar 

  • Harvell CD, Mitchell CE, Ward JR, Altizer S, Dobson AP, Ostfeld RS, Samuel MD (2002) Climate warming and disease risks for terrestrial and marine biota. Science 296:2158–2162

    Article  CAS  Google Scholar 

  • Hedayati M, Pasqualotto A, Warn P, Bowyer P, Denning D (2007) Aspergillus flavus: human pathogen, allergen and mycotoxin producer. Microbiology 153:1677–1692

    Article  CAS  Google Scholar 

  • Hoegh-Guldberg O, Bruno JF (2010) The impact of climate change on the world’s marine ecosystems. Science 328:1523–1528

    Article  CAS  Google Scholar 

  • Hoge R, Pelzer A, Rosenau F, Wilhelm S (2010) Current research, technology and education topics in applied microbiology and microbial biotechnology. In: Mendez-Vilas A (ed) Weapons of a pathogen: proteases and their role in virulence of Pseudomonas aeruginosa. Formatex Research Center, Badajoz

    Google Scholar 

  • Jongsma MA, Bolter C (1997) The adaptation of insects to plant protease inhibitors. J Insect Physiol 43:885–895

    Article  CAS  Google Scholar 

  • Kim K, Harvell CD (2004) The rise and fall of a six-year coral-fungal epizootic. Am Nat 164:S52–S63

    Article  Google Scholar 

  • Kim J-Y, Park S-C, Hwang I, Cheong H, Nah J-W, Hahm K-S, Park Y (2009) Protease inhibitors from plants with antimicrobial activity. Int J Mol Sci 10:2860–2872

    Article  CAS  Google Scholar 

  • Krull R, Cordes C, Horn H, Kampen I, Kwade A, Neu TR, Nörtemann B (2010) Morphology of filamentous fungi: linking cellular biology to process engineering using Aspergillus niger biosystems engineering II. Springer, Heidelberg, pp 1–21

    Google Scholar 

  • Kulshrestha V, Pathak S (1997) Aspergillosis in German cockroach Blattella germanica (L.)(Blattoidea: blattellidae). Mycopathologia 139:75–78

    Article  CAS  Google Scholar 

  • Lee CY, Cheng MF, Yu MS, Pan MJ (2002) Purification and characterization of a putative virulence factor, serine protease, from Vibrio parahaemolyticus. FEMS Microbiol Lett 209:31–37

    Article  CAS  Google Scholar 

  • Little TJ, Hultmark D, Read AF (2005) Invertebrate immunity and the limits of mechanistic immunology. Nat Immunol 6:651–654

    Article  CAS  Google Scholar 

  • McGillivray SM, Tran DN, Ramadoss NS, Alumasa JN, Okumura CY, Sakoulas G, Vaughn MM, Zhang DX, Keiler KC, Nizet V (2012) Pharmacological inhibition of the clpxp protease increases bacterial susceptibility to host cathelicidin antimicrobial peptides and cell envelope-active antibiotics. Antimicrob Agents Chemother 56:1854–1861

    Article  CAS  Google Scholar 

  • McManus M, White DR, McGregor P (1994) Accumulation of a chymotrypsin inhibitor in transgenic tobacco can affect the growth of insect pests. Transgenic Res 3:50–58. doi:10.1007/BF01976027

    Article  CAS  Google Scholar 

  • Monod M, Capoccia S, Lechenne B, Zaugg C, Holdom M, Jousson O (2002) Secreted proteases from pathogenic fungi. Int J Med Microbiol 292:405–419

    Article  CAS  Google Scholar 

  • Mydlarz LD, Harvell CD (2007) Peroxidase activity and inducibility in the sea fan coral exposed to a fungal pathogen. Comp Biochem Physiol A Mol Integr Physiol 146:54–62

    Article  Google Scholar 

  • Mydlarz LD, Holthouse SF, Peters EC, Harvell CD (2008) Cellular responses in sea fan corals: granular amoebocytes react to pathogen and climate stressors. Plos One 3(3):e1811. doi:10.1371/journal.pone.0001811

    Article  Google Scholar 

  • Mydlarz LD, McGinty ES, Harvell CD (2010) What are the physiological and immunological responses of coral to climate warming and disease? J Exp Biol 213:934–945

    Article  Google Scholar 

  • Novillo C, Castañera P, Ortego F (1997) Inhibition of digestive trypsin-like proteases from larvae of several lepidopteran species by the diagnostic cysteine protease inhibitor E-64. Insect Biochem Mol Biol 27:247–254

    Article  CAS  Google Scholar 

  • Palmer CV, McGinty ES, Cummings DJ, Smith SM, Bartels E, Mydlarz LD (2011) Patterns of coral ecological immunology: variation in the responses of Caribbean corals to elevated temperature and a pathogen elicitor. J Exp Biol 214:4240–4249

    Article  CAS  Google Scholar 

  • Pandolfi JM, Connolly SR, Marshall DJ, Cohen AL (2011) Projecting coral reef futures under global warming and ocean acidification. Science 333:418–422

    Article  CAS  Google Scholar 

  • Petes LE, Harvell CD, Peters EC, Webb MAH, Mullen KM (2003) Pathogens compromise reproduction and induce melanization in Caribbean sea fans. Mar Ecol Prog Ser 264:167–171

    Article  Google Scholar 

  • Rahim MA, Bakhiet AO, Hussein MF (2013) Aspergillosis in a gyrfalcon (Falco rusticolus) in Saudi Arabia. Comp Clin Pathol 22:131–135

    Article  Google Scholar 

  • Rolff J, Siva-Jothy MT (2003) Invertebrate ecological immunology. Science 301:472–475. doi:10.1126/science.1080623

    Article  CAS  Google Scholar 

  • Ruiz-Morenol D, Willis BL, Page AC, Weil E, Cróquer A, Vargas-Angel B, Jordan-Garza AnG, Jordán-Dahlgren E, Raymund L, Harvell CD (2012) Global coral disease prevalence associated with sea temperature anomalies and local factors. Dis Aquat Org 100:249–261

    Article  Google Scholar 

  • Rypien KL, Andras JP (2008) Isolation and characterization of microsatellite loci in Aspergillus sydowii, a pathogen of Caribbean sea fan corals. Mol Ecol Res 8:230–232

    Article  CAS  Google Scholar 

  • Rypien KL, Andras JP, Harvell C (2008) Globally panmictic population structure in the opportunistic fungal pathogen Aspergillus sydowii. Mol Ecol 17:4068–4078

    Article  Google Scholar 

  • Schomburg I, Chang A, Placzek S, Söhngen C, Rother M, Lang M, Munaretto C, Ulas S, Stelzer M, Grote A, Scheer M, Schomburg D (2013) BRENDA in 2013: integrated reactions, kinetic data, enzyme function data, improved disease classification: new options and contents in BRENDA. Nucleic Acids Res 41(Database issue):D764–D772

  • Sugumaran M, Saul SJ, Ramesh N (1985) Endogenous protease inhibitors prevent undesired activation of prophenoloxidase in insect hemolymph. Biochem Biophys Res Commun 132:1124–1129. doi:10.1016/0006-291X(85)91923-0

  • Sunde J, Taranger G, Rungruangsak-Torrissen K (2001) Digestive protease activities and free amino acids in white muscle as indicators for feed conversion efficiency and growth rate in Atlantic salmon (Salmo salar L.). Fish Physiol Biochem 25:335–345

    Article  Google Scholar 

  • Twining SS (1984) Fluorescein isothiocyanate-labeled casein assay for proteolytic enzymes. Anal Biochem 143:30–34

    Article  CAS  Google Scholar 

  • Van de Ven WJ, Roebroek AJ, Van Duijnhoven HL (1993) Structure and function of eukaryotic proprotein processing enzymes of the subtilisin family of serine proteases. Crit Rev Oncogen 4:115–136

    Google Scholar 

  • Wang S-L, Chen Y-H, Yen Y-H (2005) Purification and characterization of a serine protease extracellularly produced by Aspergillus fumigatus in a shrimp and crab shell powder medium. Enzyme Microb Technol 36:660–665

    Article  CAS  Google Scholar 

  • Ward JR, Kim K, Harvell C (2007) Temperature affects coral disease resistance and pathogen growth. Mar Ecol Prog Ser 329:115–121

    Article  Google Scholar 

  • Weiss Y, Forêt S, Hayward DC, Ainsworth T, King R, Ball EE, Miller DJ (2013) The acute transcriptional response of the coral Acropora millepora to immune challenge: expression of GiMAP/IAN genes links the innate immune responses of corals with those of mammals and plants. BMC Genom 14:400

    Article  CAS  Google Scholar 

  • Xue Q-G, Waldrop GL, Schey KL, Itoh N, Ogawa M, Cooper RK, Losso JN, La Peyre JF (2006) A novel slow-tight binding serine protease inhibitor from eastern oyster (Crassostrea virginica) plasma inhibits perkinsin, the major extracellular protease of the oyster protozoan parasite Perkinsus marinus. Comp Biochem Physiol B 145:16–26

    Article  Google Scholar 

Download references

Acknowledgments

Research was funded and supported by NSF (OCE-0849799). The authors would like to thank Ernesto Weil (University of Puerto Rico) and Eric Bartels (Mote Marine Laboratory) for aiding in the collection process, field assistance, and transfer of the coral specimens back to the University of Texas at Arlington. We also thank Lindsey Dornberger and April Klein (undergraduates at UTA) for their help with the processing of the sea fan samples and Colleen Burge (Cornell University) for discussions. We also thank the reviewers for valuable comments which considerably improved this manuscript. All samples were collected under Florida Keys National Marine Sanctuary Permit No. 2004-092 and under the specification of research collection permits to the Department of Marine Science UPRM.

Author information

Authors and Affiliations

  1. The University of Texas at Arlington, 501 S. Nedderman, Life Science 337, Arlington, TX, 76019, USA

    Whitney T. Mann, Joshuah Beach-Letendre & Laura D. Mydlarz

Authors
  1. Whitney T. Mann
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Joshuah Beach-Letendre
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Laura D. Mydlarz
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Laura D. Mydlarz.

Additional information

Communicated by T. Reusch.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Mann, W.T., Beach-Letendre, J. & Mydlarz, L.D. Interplay between proteases and protease inhibitors in the sea fan—Aspergillus pathosystem. Mar Biol 161, 2213–2220 (2014). https://doi.org/10.1007/s00227-014-2499-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00227-014-2499-2

Keywords

Search

Navigation