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The Role of Fungi and Bactria on the Organic Matter THE ROLE OF FUNGI AND BACTERIA ON THE ORGANIC MATTER DECOMPOSITION PROCESS IN STREAMS: INTERACTION AND RELEVANCE IN BIOFILMS Joan ARTIGAS ALEJO ISBN: 978-84-692-2181-5 Dipòsit legal: GI-355-2009 Facultat de Ciències Institut d’Ecologia Aquàtica THE ROLE OF FUNGI AND BACTERIA ON THE ORGANIC MATTER DECOMPOSITION PROCESS IN STREAMS: INTERACTION AND RELEVANCE IN BIOFILMS Memòria presentada per Joan Artigas i Alejo per optar al grau de Doctor per la Universitat de Girona Vist-i-plau dels directors: El doctorand: Dr. Sergi Sabater Cortés Dra. Anna M. Romaní Cornet Joan Artigas Alejo Institut d’Ecologia Aquàtica Institut d’Ecologia Aquàtica Universitat de Girona Universitat de Girona Girona, Novembre 2008 AGRAÏMENTS És molta la gent que m’ha ajudat a tirar endavant aquest treball i espero no oblidar- me’n de cap! En primer lloc, gràcies Anna i Sergi per haver-me obert aquesta porta, haver-me ensenyat el que sabeu i haver-me contagiat el vostre entusiasme. Gràcies a la meva família (la mare, el pare i en Narcís) perquè sempre m’heu donat suport i cregut amb el que estava fent, tot i que a vegades us ho expliqués fatal. I sobretot, gràcies Carlitus per ser-hi tu i la resta de la família (el Paco, la Lluna i la Nelly), per interessar-te i preguntar-me coses de la feina i sobretot per escoltar-me quan tenia un problema. Gràcies a la meva medicina particular, el patinatge, perquè m’ha ajudat a fer complets resets dels problemassos i anades d’olla que es tenen en el “dia a dia” de la tesi. Sense l’ajuda de tots vosaltres, aquest treball no hagués estat possible. Floretes Sandra i Bet, vam començar fa molts anys! No diré quan… Hem viscut moltes coses junts! Gràcies per haver-hi sigut, sense vosaltres la tesi no hagués tingut el mateix gust. Irene veïna de taula, hem rigut molt i hem pencat molt! Un xin-xin per l’Ebre! Podria seguir fent comentaris de tots i cadascun perquè ja sabeu que quan m’hi poso puc batejar de nou “la Verge de la pota arrossegada”. Però no seria el cas, perquè quan obro la boca “puja el preu del pa”. Gràcies companys del FLUECO team (Helena, Marta, Berta, Natàlia, Chloe, Leslie, Lorenzo, Anita, Francesco, Xisca, Susanna, Gemma U i Gemma V). Ups, me n’oblidava dels companys de la UB (Ainoha, Rut, Isabel, Isis, Julio)! Gent, ens les hem vist i desitjat quan la Tordera anava com les cabres i quan Fuirosos estava fred com el glaç. Lo millor de tot el dia “inuncat”, amb la Clara, l’Anna i el del tractor remolcador… encara al.lucino de la situació. No menys important ha sigut el suport i “bon rotllo” que he rebut de la resta de gent de l’Àrea d’Ecologia. Aiguamollerus i peixòlegs sou uns cracks tots plegats. Diuen que la recerca ha de ser “interdisciplinar”, doncs merci genètics, micros, bio cel.lulars, zoòlegs per aquells favorets i per les bones estones del dinar. Aquesta tesi ha estat finançada pels següents projectes: Patterns of biofilm formation: changes in community structure and metabolism under different light and temperature conditions (HA2004-0020) del MEC, Efectos de episodios de interrupción del flujo sobre la continuidad estructural y funcional de sistemas fluviales (CGL2007- 65549/BOS) del CICYT i Cambios globales en sistemas fluviales: efectos sobre la biodiversidad, la red trófica y el funcionamiento del sistema (GLOBRIO) de la FBBVA. També he gaudit d’una beca predoctoral BR concedida per la Universitat de Girona. Això de fer la tesi ha sigut molt “xulo”! 1 2 INDEX Summary 5-6 Resum (in Catalan) 7-8 General introduction 9-20 Materials and Methods 21-42 Chapter 1. Organic matter availability structures microbial biomass and 43-56 activity in a Mediterranean stream Chapter 2. Organic matter decomposition by fungi in a Mediterranean 57-70 forested stream: contribution of streambed substrata Chapter 3. Relating nutrient molar ratios of microbial attached 71-84 communities to organic matter utilization in a forested stream Chapter 4. Relationships between microbial biomass and extracellular 85-102 enzyme activities during leaf litter breakdown in a forested stream Chapter 5. Patterns of epilithic biofilm formation in two streams 103-122 belonging to different bioclimatic regions: analysis on microbial community structure and metabolism Chapter 6. Relevance of polymeric matrix enzymes during biofilm 123-140 formation Chapter 7. Effect of nutrients on the sporulation and diversity of aquatic 141-154 hyphomycetes on submerged substrata in a Mediterranean stream Chapter 8. Effect of water nutrient concentration and N:P molar ratio on 155-170 biofilm structure and metabolism Aquatic microbial ecology: new trends and future perspectives 171-172 References 173-194 Conclusions 195-199 3 4 Summary SUMMARY The microbial structure and metabolism of benthic microbial communities was analyzed over a hydrological year in a Mediterranean forested stream (the Fuirosos). Microbial heterotrophic biomass (bacteria plus fungi) was generally higher than autotrophic biomass (algae), except during short periods of high light availability in the spring and winter. During these periods, algal biomass and peptidase activity increased in benthic communities. Heterotrophic biomass and activity (polysaccharide and lignin degrading activities) showed a peak in autumn. The Mediterranean summer drought provoked an earlier leaf fall. The resumption of the water flow caused the weathering of riparian soils and subsequently a large increase in dissolved organic carbon and nitrate, which led to growth of bacteria and fungi. The aquatic microfungi in the Fuirosos mainly developed in leaves, but were also relevant in sand and gravel habitats. In general, the enzymatic activities of microbial communities were linked to their nutrient molar ratios (biofilm C:N and N:P) and, at the same time, these ratios might be modulated by the different nature of available organic matter in each substratum and by the water nutrient concentrations. According to this, microbial communities associated to leaves and branches showed higher C: N and lower N: P molar ratios and higher polysaccharide degrading activity. Instead, biofilms on sand and gravel, where algae accumulated and fine detritic materials were more available, showed lower C: N and higher N: P molar ratios, as well as higher ligninolytic and peptidase activity. Leaf litter colonization and breakdown in streams is mostly carried out by fungi. A three-month litter breakdown experiment using two different leaf species (Platanus acerifolia and Populus nigra) revealed different patterns of fungal and bacterial biomass accumulation. Bacteria increased earlier than fungi in leaves, though fungi prevailed in terms of biomass and activity. The widest and fastest leaf structural changes and the maximum enzyme activities per unit of microbial carbon took place between the second and third week of experiment. There was an exponential relationship between bacterial biomass and most of the enzyme activities measured in the two leaf species. However, this relationship was consistent between fungal biomass and activities only in the Platanus leaves, which has the lowest breakdown rate. These results suggest that fungi probably required of a higher stability than bacteria to develop and to degrade substrates. In contrast to leaf communities, stream epilithic biofilms (communities growing on rocky substrata) are mainly colonized by algae, bacteria and protozoa. Patterns on epilithic biofilm formation in two streams of different bioclimatic regions (a Central 5 Summary European, the Walzbach and a Mediterranean, the Fuirosos) were related to environmental characteristics. Flooding episodes produced a drastic reset in diatom populations in the Fuirosos. Overall, the higher structural complexity of the epilithic biofilms in the Mediterranean stream (higher bacterial biodiversity and biomass and extracellular polysaccharide content) did not result on major enzyme activity efficiency per bacterial cell. Conversely, the environmental stability in the Central European stream played an important role in shaping biofilm structure and in regulating a more efficient use of the organic matter resources. Deriving from this experiment, an extraction analysis using a cation exchange resin was optimized to measure matrix- enzymes (those included in the extrapolymeric substances matrix) in freshwater biofilms. Analysis of extracellular enzyme activity distinguishing enzyme activity in EPS matrix (matrix-enzymes) and total biofilm extracellular enzyme activity (undisrupted biofilm) revealed that matrix-enzymes accounted for 65-81% of total biofilm enzyme activity, though matrix-enzyme activity decreased as biofilm matured. Nutrient enrichment in streams often results in enhanced decomposition rates and chemical conditions that affect the suitability of the habitat for benthic communities. With this purpose, two nutrient enrichment experiments (nitrate and phosphate addition) were conducted on benthic microbial communities to determine: i) whether long- and short-term (1.5 years and 48h, respectively) nutrient enrichment affected sporulation and diversity of aquatic hyphomycetes, and ii) whether changes in total water nutrient concentration and N:P molar ratios affected epilithic biofilms integrity. Long-term nutrient additions did not affect potential sporulation rates, though short-term nutrient additions produced insignificant increases in these rates. However, long-term nutrient enrichment produced significant changes in the hyphomycetes community composition. Further, biofilms exposed to high water nutrient concentration showed
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