Soil and Rhizosphere Associated Fungi in Gray Mangroves(Avicennia marina) from the Red Sea—A Metagenomic Approach
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摘要
Covering a quarter of the world's tropical coastlines and being one of the most threatened ecosystems, mangroves are among the major sources of terrestrial organic matter to oceans and harbor a wide microbial diversity. In order to protect, restore, and better understand these ecosystems, researchers have extensively studied their microbiology, yet few surveys have focused on their fungal communities. Our lack of knowledge is even more pronounced for specific fungal populations, such as the ones associated with the rhizosphere. Likewise, the Red Sea gray mangroves(Avicennia marina) remain poorly characterized, and understanding of their fungal communities still relies on cultivation-dependent methods. In this study, we analyzed metagenomic datasets from gray mangrove rhizosphere and bulk soil samples collected in the Red Sea coast, to obtain a snapshot of their fungal communities. Our data indicated that Ascomycota was the dominant phylum(76%–85%), while Basidiomycota was less abundant(14%–24%), yet present in higher numbers than usually reported for such environments. Fungal communities were more stable within the rhizosphere than within the bulk soil, both at class and genus level. This finding is consistent with the intrinsic patchiness in soil sediments and with the selection of specific microbial communities by plant roots. Our study indicates the presence of several species on this mycobiome that were not previously reported as mangrove-associated. In particular, we detected representatives of several commercially-used fungi, e.g., producers of secreted cellulases and anaerobic producers of cellulosomes. These results represent additional insights into the fungal community of the gray mangroves of the Red Sea, and show that they are significantly richer than previously reported.
Covering a quarter of the world's tropical coastlines and being one of the most threatened ecosystems, mangroves are among the major sources of terrestrial organic matter to oceans and harbor a wide microbial diversity. In order to protect, restore, and better understand these ecosystems, researchers have extensively studied their microbiology, yet few surveys have focused on their fungal communities. Our lack of knowledge is even more pronounced for specific fungal populations, such as the ones associated with the rhizosphere. Likewise, the Red Sea gray mangroves(Avicennia marina) remain poorly characterized, and understanding of their fungal communities still relies on cultivation-dependent methods. In this study, we analyzed metagenomic datasets from gray mangrove rhizosphere and bulk soil samples collected in the Red Sea coast, to obtain a snapshot of their fungal communities. Our data indicated that Ascomycota was the dominant phylum(76%–85%), while Basidiomycota was less abundant(14%–24%), yet present in higher numbers than usually reported for such environments. Fungal communities were more stable within the rhizosphere than within the bulk soil, both at class and genus level. This finding is consistent with the intrinsic patchiness in soil sediments and with the selection of specific microbial communities by plant roots. Our study indicates the presence of several species on this mycobiome that were not previously reported as mangrove-associated. In particular, we detected representatives of several commercially-used fungi, e.g., producers of secreted cellulases and anaerobic producers of cellulosomes. These results represent additional insights into the fungal community of the gray mangroves of the Red Sea, and show that they are significantly richer than previously reported.
Covering a quarter of the world's tropical coastlines and being one of the most threatened ecosystems, mangroves are among the major sources of terrestrial organic matter to oceans and harbor a wide microbial diversity. In order to protect, restore, and better understand these ecosystems, researchers have extensively studied their microbiology, yet few surveys have focused on their fungal communities. Our lack of knowledge is even more pronounced for specific fungal populations, such as the ones associated with the rhizosphere. Likewise, the Red Sea gray mangroves(Avicennia marina) remain poorly characterized, and understanding of their fungal communities still relies on cultivation-dependent methods. In this study, we analyzed metagenomic datasets from gray mangrove rhizosphere and bulk soil samples collected in the Red Sea coast, to obtain a snapshot of their fungal communities. Our data indicated that Ascomycota was the dominant phylum(76%–85%), while Basidiomycota was less abundant(14%–24%), yet present in higher numbers than usually reported for such environments. Fungal communities were more stable within the rhizosphere than within the bulk soil, both at class and genus level. This finding is consistent with the intrinsic patchiness in soil sediments and with the selection of specific microbial communities by plant roots. Our study indicates the presence of several species on this mycobiome that were not previously reported as mangrove-associated. In particular, we detected representatives of several commercially-used fungi, e.g., producers of secreted cellulases and anaerobic producers of cellulosomes. These results represent additional insights into the fungal community of the gray mangroves of the Red Sea, and show that they are significantly richer than previously reported.
引文
[1]Arfi Y,Buee M,Marchand C,Levasseur A,Record E.Multiple markers pyrosequencing reveals highly diverse and host-specific fungal communities on the mangrove trees Avicennia marina and Rhizophora stylosa.FEMS Microbiol Immunol 2012;79:433–44.
[2]Ghizelini AM,Mendonc?a-Hagler LCS,Macrae A.Microbial diversity in Brazilian mangrove sediments:a mini review.Braz J Microbiol 2012;43:1242–54.
[3]Shearer CA,Descals E,Kohlmeyer B,Kohlmeyer J,MarvanovaL,Padgett D,et al.Fungal biodiversity in aquatic habitats.Biodivers Conserv 2007;16:49–67.
[4]Mendes R,Garbeva P,Raaijmakers JM.The rhizosphere microbiome:significance of plant beneficial,plant pathogenic,and human pathogenic microorganisms.FEMS Microbiol Rev2013;37:634–63.
[5]Alongi DM.Bacterial productivity and microbial biomass in tropical mangrove sediments.Microb Ecol 1988;15:59–79.
[6]Simoes MF,Pereira L,Santos C,Lima N.Polyphasic identification and preservation of fungal diversity:concepts and applications.In:Malik A,Grohmann E,Alves M,editors.Management of microbial resources in the environment.Dordrecht,Netherlands:Springer;2013.p.91–117.
[7]Liu P,Wang XH,Li JG,Qin W,Xiao CZ,Zhao X,et al.Pyrosequencing reveals fungal communities in the rhizosphere of Xinjiang jujube.Biomed Res Int 2015;2015:972481.
[8]Arfi Y,Marchand C,Wartel M,Record E.Fungal diversity in anoxic-sulfidic sediments in a mangrove soil.Fungal Ecol2012;5:282–5.
[9]Abdel-Wahab MA,Hodhod MS,Bahkali AH,Jones EB.Marine fungi of Saudi Arabia.Bot Mar 2014;57:323–35.
[10]Alsheikh-Hussain A,Altenaiji EM,Yousef LF.Fungal cellulases from mangrove forests—a short review.J Biochem Technol2014;5:765–74.
[11]Sarma VV,Hyde KD.A review on frequently occurring fungi in mangroves.Fungal Divers 2001;8:1–34.
[12]Alias SA,Zainuddin N,Jones EB.Biodiversity of marine fungi in Malaysian mangroves.Bot Mar 2010;53:545–54.
[13]Schmit JP,Shearer CA.A checklist of mangrove-associated fungi,their geographical distribution and known host plants.Mycotaxon 2003;85:423–77.
[14]Alongi DM.5.Mangrove–Microbe–Soil Relations.In:Kristensen E,Haese RR,Kostka JE,editors.Interactions between macroand microorganisms in marine sediments.American Geophysical Union;2005.p.85–103.
[15]Nambiar GR,Raveendran K.Manglicolous marine fungi on Avicennia and Rhizophora along Kerala coast(India).Middle East J Sci Res 2009;4:48–51.
[16]Lee BK,Baker GE.Fungi associated with the roots of red mangrove.Rhizophora mangle.Mycologia 1973;65:894–906.
[17]Selvakumar V,Panneerselvam A,Vijayakumar N,Savery MA,Thajuddin N.Diversity of endophytic and rhizosphere soil fungi of Avicennia marina in Maravakadu Mangrove Forest.IOSR J Pharm Biol Sci 2014;9:24–8.
[18]Thiripurasundari G,Usharani G,Parthasarathi R,Neelakandan T.Microbial diversity of the rhizosphere soil of Avicennia marina and Avicennia officinalis collected from mangrove forest.Int J Recent Sci Res 2010;1:039–41.
[19]Kennedy J,Flemer B,Jackson SA,Lejon DP,Morrissey JP,O’gara F,et al.Marine metagenomics:new tools for the study and exploitation of marine microbial metabolism.Mar Drugs2010;8:608–28.
[20]Cuadros-Orellana S,Leite LR,Smith A,Medeiros JD,Badotti F,Fonseca PLC,et al.Assessment of fungal diversity in the environment using metagenomics:a decade in review.Fungal Genom Biol 2013;3:110.
[21]Guo X,Zhang Q,Zhang X,Zhang J,Gong J.Marine fungal communities in water and surface sediment of a sea cucumber farming system:habitat-differentiated distribution and nutrients driving succession.Fungal Ecol 2015;14:87–98.
[22]Robitzch V,Banguera-Hinestroza E,Sawall Y,Al-Sofyani A,Voolstra CR.Absence of genetic differentiation in the coral Pocillopora verrucosa along environmental gradients of the Saudi Arabian Red Sea.Front Mar Sci 2015.http://dx.doi.org/10.3389/fmars.2015.00005.
[23]Khan M,Kumar A,Muqtadir A.Distribution of mangroves along the Red Sea coast of the Arabian Peninsula:Part 2.The southern coast of western Saudi Arabia.e-Journal Earth Sci India2010;3:154–62.
[24]Kumar A,Khan MA,Muqtadir A.Distribution of mangroves along the Red Sea coast of the Arabian Peninsula:Part-I:the northern coast of western Saudi Arabia.e-Journal Earth Sci India2010;3:2842.
[25]PERSGA/GEF.Status of mangroves in the Red Sea and Gulf of Aden.PERSGA Technical Series No.11,PERSGA,Jeddah;2004.http://www.persga.org/Documents/Mangroves_Status.pdf.
[26]Price ARG,Medley PAH,Mc Dowall RJ,Dawson-Shepherd AR,Hogarth PJ,Ormond RFG.Aspects of mangal ecology along the Red Sea coast of Saudi Arabia.J Nat Hist 1987;21:449–64.
[27]Cheng ZS,Pan JH,Tang WC,Chen QJ,Lin YC.Biodiversity and biotechnological potential of mangrove-associated fungi.J For Res 2009;20:63–72.
[28]Sridhar KR.Mangrove fungi in India.Curr Sci 2004;86:1586–7.
[29]Kuramae EE,Yergeau E,Wong LC,Pijl AS,van Veen JA,Kowalchuk GA.Soil characteristics more strongly influence soil bacterial communities than land-use type.FEMS Microbiol Ecol2012;79:12–24.
[30]Hyde KD,Lee SY.Ecology of mangrove fungi and their role in nutrient cycling:what gaps occur in our knowledge?Hydrobiologia 1995;295:107–18.
[31]Reef R,Feller IC,Lovelock CE.Nutrition of mangroves.Tree Physiol 2010;30:1148–60.
[32]Ngugi DK,Antunes A,Brune A,Stingl U.Biogeography of pelagic bacterioplankton across an antagonistic temperature—salinity gradient in the Red Sea.Mol Ecol 2012;21:388–405.
[33]Velez P,Gonzalez MC,Rosique-Gil E,Cifuentes J,del Roc?o Reyes-Montes M,Capello-Garc?a S,et al.Community structure and diversity of marine ascomycetes from coastal beaches of the southern Gulf of Mexico.Fungal Ecol 2013;6:513–21.
[34]Mandeel QA.Microfungal community associated with rhizosphere soil of Zygophyllum qatarense in arid habitats of Bahrain.J Arid Environ 2002;50:665–81.
[35]Edgcomb VP,Beaudoin D,Gast R,Biddle JF,Teske A.Marine subsurface eukaryotes:the fungal majority.Environ Microbiol2011;13:172–83.
[36]Abdel-Azeem AM,Salem FM.Biodiversity of laccase producing fungi in Egypt.Mycosphere 2012;3:900–20.
[37]Richards TA,Jones MD,Leonard G,Bass D.Marine fungi:their ecology and molecular diversity.Ann Rev Mar Sci2012;4:495–522.
[38]Lauber CL,Strickland MS,Bradford MA,Fierer N.The influence of soil properties on the structure of bacterial and fungal communities across land-use types.Soil Biol Biochem2008;40:2407–15.
[39]Petrescu-Da?nila?E,Voicu M,Sta?nescu R,Stoica B,Rusu M.Fission yeast Schizosaccharomyces pombe as a producer and secretor of heterologous proteins.Rom Biotechnol Lett2009;14:4201–10.
[40]Oda K,Kakizono D,Yamada O,Iefuji H,Akita O,Iwashita K.Proteomic analysis of extracellular proteins from Aspergillus oryzae grown under submerged and solid-state culture conditions.Appl Environ Microbiol 2006;72:3448–57.
[41]Takegawa K,Tohda H,Sasaki M,Idiris A,Ohashi T,Mukaiyama H,et al.Production of heterologous proteins using the fission-yeast(Schizosaccharomyces pombe)expression system.Biotechnol Appl Biochem 2009;53:227–35.
[42]Jones EBG,Sakayaroj J,Suetrong S,Somrithipol S,Pang KL.Classification of marine Ascomycota,anamorphic taxa and Basidiomycota.Fungal Divers 2009;35:1–187.
[43]Thamizhmani R,Senthilkumaran R.Diversity of fungi in selected mangroves along the east coast of India.Int J Curr Microbiol Appl Sci 2012;1:29–33.
[44]Sahoo K,Dhal NK.Potential microbial diversity in mangrove ecosystems:a review.Indian J Marine Sci 2009;38:249–56.
[45]Alzubaidy H,Essack M,Malas TB,Bokhari A,Motwalli O,Kamanu FK,et al.Rhizosphere microbiome metagenomics of gray mangroves(Avicennia marina)in the Red Sea.Gene 2015.http://dx.doi.org/10.1016/j.gene.2015.10.032.
[46]Dean WE.Determination of carbonate and organic matter in calcareous sediments and sedimentary rocks by loss on ignition:comparison with other methods.J Sed Petrol 1974;44:242–8.
[47]Meyer F,Paarmann D,D’Souza M,Olson R,Glass EM,Kubal M,et al.The metagenomics RAST serve:a public resource for the automatic phylogenetic and functional analysis of metagenomes.BMC Bioinformatics 2008;9:386–94.
[48]Zak JC,Willig MR.Fungal biodiversity patterns.In:Mueller G,Foster M,Bills G,editors.Biodiversity of fungi:inventory and monitoring methods.Amsterdam:Academic Press;2004.p.59–75.
[49]Parks DH,Tyson GW,Hugenholtz P,Beiko RG.STAMP:statistical analysis of taxonomic and functional profiles.Bioinformatics 2014;30:3123–4.
[2]Ghizelini AM,Mendonc?a-Hagler LCS,Macrae A.Microbial diversity in Brazilian mangrove sediments:a mini review.Braz J Microbiol 2012;43:1242–54.
[3]Shearer CA,Descals E,Kohlmeyer B,Kohlmeyer J,MarvanovaL,Padgett D,et al.Fungal biodiversity in aquatic habitats.Biodivers Conserv 2007;16:49–67.
[4]Mendes R,Garbeva P,Raaijmakers JM.The rhizosphere microbiome:significance of plant beneficial,plant pathogenic,and human pathogenic microorganisms.FEMS Microbiol Rev2013;37:634–63.
[5]Alongi DM.Bacterial productivity and microbial biomass in tropical mangrove sediments.Microb Ecol 1988;15:59–79.
[6]Simoes MF,Pereira L,Santos C,Lima N.Polyphasic identification and preservation of fungal diversity:concepts and applications.In:Malik A,Grohmann E,Alves M,editors.Management of microbial resources in the environment.Dordrecht,Netherlands:Springer;2013.p.91–117.
[7]Liu P,Wang XH,Li JG,Qin W,Xiao CZ,Zhao X,et al.Pyrosequencing reveals fungal communities in the rhizosphere of Xinjiang jujube.Biomed Res Int 2015;2015:972481.
[8]Arfi Y,Marchand C,Wartel M,Record E.Fungal diversity in anoxic-sulfidic sediments in a mangrove soil.Fungal Ecol2012;5:282–5.
[9]Abdel-Wahab MA,Hodhod MS,Bahkali AH,Jones EB.Marine fungi of Saudi Arabia.Bot Mar 2014;57:323–35.
[10]Alsheikh-Hussain A,Altenaiji EM,Yousef LF.Fungal cellulases from mangrove forests—a short review.J Biochem Technol2014;5:765–74.
[11]Sarma VV,Hyde KD.A review on frequently occurring fungi in mangroves.Fungal Divers 2001;8:1–34.
[12]Alias SA,Zainuddin N,Jones EB.Biodiversity of marine fungi in Malaysian mangroves.Bot Mar 2010;53:545–54.
[13]Schmit JP,Shearer CA.A checklist of mangrove-associated fungi,their geographical distribution and known host plants.Mycotaxon 2003;85:423–77.
[14]Alongi DM.5.Mangrove–Microbe–Soil Relations.In:Kristensen E,Haese RR,Kostka JE,editors.Interactions between macroand microorganisms in marine sediments.American Geophysical Union;2005.p.85–103.
[15]Nambiar GR,Raveendran K.Manglicolous marine fungi on Avicennia and Rhizophora along Kerala coast(India).Middle East J Sci Res 2009;4:48–51.
[16]Lee BK,Baker GE.Fungi associated with the roots of red mangrove.Rhizophora mangle.Mycologia 1973;65:894–906.
[17]Selvakumar V,Panneerselvam A,Vijayakumar N,Savery MA,Thajuddin N.Diversity of endophytic and rhizosphere soil fungi of Avicennia marina in Maravakadu Mangrove Forest.IOSR J Pharm Biol Sci 2014;9:24–8.
[18]Thiripurasundari G,Usharani G,Parthasarathi R,Neelakandan T.Microbial diversity of the rhizosphere soil of Avicennia marina and Avicennia officinalis collected from mangrove forest.Int J Recent Sci Res 2010;1:039–41.
[19]Kennedy J,Flemer B,Jackson SA,Lejon DP,Morrissey JP,O’gara F,et al.Marine metagenomics:new tools for the study and exploitation of marine microbial metabolism.Mar Drugs2010;8:608–28.
[20]Cuadros-Orellana S,Leite LR,Smith A,Medeiros JD,Badotti F,Fonseca PLC,et al.Assessment of fungal diversity in the environment using metagenomics:a decade in review.Fungal Genom Biol 2013;3:110.
[21]Guo X,Zhang Q,Zhang X,Zhang J,Gong J.Marine fungal communities in water and surface sediment of a sea cucumber farming system:habitat-differentiated distribution and nutrients driving succession.Fungal Ecol 2015;14:87–98.
[22]Robitzch V,Banguera-Hinestroza E,Sawall Y,Al-Sofyani A,Voolstra CR.Absence of genetic differentiation in the coral Pocillopora verrucosa along environmental gradients of the Saudi Arabian Red Sea.Front Mar Sci 2015.http://dx.doi.org/10.3389/fmars.2015.00005.
[23]Khan M,Kumar A,Muqtadir A.Distribution of mangroves along the Red Sea coast of the Arabian Peninsula:Part 2.The southern coast of western Saudi Arabia.e-Journal Earth Sci India2010;3:154–62.
[24]Kumar A,Khan MA,Muqtadir A.Distribution of mangroves along the Red Sea coast of the Arabian Peninsula:Part-I:the northern coast of western Saudi Arabia.e-Journal Earth Sci India2010;3:2842.
[25]PERSGA/GEF.Status of mangroves in the Red Sea and Gulf of Aden.PERSGA Technical Series No.11,PERSGA,Jeddah;2004.http://www.persga.org/Documents/Mangroves_Status.pdf.
[26]Price ARG,Medley PAH,Mc Dowall RJ,Dawson-Shepherd AR,Hogarth PJ,Ormond RFG.Aspects of mangal ecology along the Red Sea coast of Saudi Arabia.J Nat Hist 1987;21:449–64.
[27]Cheng ZS,Pan JH,Tang WC,Chen QJ,Lin YC.Biodiversity and biotechnological potential of mangrove-associated fungi.J For Res 2009;20:63–72.
[28]Sridhar KR.Mangrove fungi in India.Curr Sci 2004;86:1586–7.
[29]Kuramae EE,Yergeau E,Wong LC,Pijl AS,van Veen JA,Kowalchuk GA.Soil characteristics more strongly influence soil bacterial communities than land-use type.FEMS Microbiol Ecol2012;79:12–24.
[30]Hyde KD,Lee SY.Ecology of mangrove fungi and their role in nutrient cycling:what gaps occur in our knowledge?Hydrobiologia 1995;295:107–18.
[31]Reef R,Feller IC,Lovelock CE.Nutrition of mangroves.Tree Physiol 2010;30:1148–60.
[32]Ngugi DK,Antunes A,Brune A,Stingl U.Biogeography of pelagic bacterioplankton across an antagonistic temperature—salinity gradient in the Red Sea.Mol Ecol 2012;21:388–405.
[33]Velez P,Gonzalez MC,Rosique-Gil E,Cifuentes J,del Roc?o Reyes-Montes M,Capello-Garc?a S,et al.Community structure and diversity of marine ascomycetes from coastal beaches of the southern Gulf of Mexico.Fungal Ecol 2013;6:513–21.
[34]Mandeel QA.Microfungal community associated with rhizosphere soil of Zygophyllum qatarense in arid habitats of Bahrain.J Arid Environ 2002;50:665–81.
[35]Edgcomb VP,Beaudoin D,Gast R,Biddle JF,Teske A.Marine subsurface eukaryotes:the fungal majority.Environ Microbiol2011;13:172–83.
[36]Abdel-Azeem AM,Salem FM.Biodiversity of laccase producing fungi in Egypt.Mycosphere 2012;3:900–20.
[37]Richards TA,Jones MD,Leonard G,Bass D.Marine fungi:their ecology and molecular diversity.Ann Rev Mar Sci2012;4:495–522.
[38]Lauber CL,Strickland MS,Bradford MA,Fierer N.The influence of soil properties on the structure of bacterial and fungal communities across land-use types.Soil Biol Biochem2008;40:2407–15.
[39]Petrescu-Da?nila?E,Voicu M,Sta?nescu R,Stoica B,Rusu M.Fission yeast Schizosaccharomyces pombe as a producer and secretor of heterologous proteins.Rom Biotechnol Lett2009;14:4201–10.
[40]Oda K,Kakizono D,Yamada O,Iefuji H,Akita O,Iwashita K.Proteomic analysis of extracellular proteins from Aspergillus oryzae grown under submerged and solid-state culture conditions.Appl Environ Microbiol 2006;72:3448–57.
[41]Takegawa K,Tohda H,Sasaki M,Idiris A,Ohashi T,Mukaiyama H,et al.Production of heterologous proteins using the fission-yeast(Schizosaccharomyces pombe)expression system.Biotechnol Appl Biochem 2009;53:227–35.
[42]Jones EBG,Sakayaroj J,Suetrong S,Somrithipol S,Pang KL.Classification of marine Ascomycota,anamorphic taxa and Basidiomycota.Fungal Divers 2009;35:1–187.
[43]Thamizhmani R,Senthilkumaran R.Diversity of fungi in selected mangroves along the east coast of India.Int J Curr Microbiol Appl Sci 2012;1:29–33.
[44]Sahoo K,Dhal NK.Potential microbial diversity in mangrove ecosystems:a review.Indian J Marine Sci 2009;38:249–56.
[45]Alzubaidy H,Essack M,Malas TB,Bokhari A,Motwalli O,Kamanu FK,et al.Rhizosphere microbiome metagenomics of gray mangroves(Avicennia marina)in the Red Sea.Gene 2015.http://dx.doi.org/10.1016/j.gene.2015.10.032.
[46]Dean WE.Determination of carbonate and organic matter in calcareous sediments and sedimentary rocks by loss on ignition:comparison with other methods.J Sed Petrol 1974;44:242–8.
[47]Meyer F,Paarmann D,D’Souza M,Olson R,Glass EM,Kubal M,et al.The metagenomics RAST serve:a public resource for the automatic phylogenetic and functional analysis of metagenomes.BMC Bioinformatics 2008;9:386–94.
[48]Zak JC,Willig MR.Fungal biodiversity patterns.In:Mueller G,Foster M,Bills G,editors.Biodiversity of fungi:inventory and monitoring methods.Amsterdam:Academic Press;2004.p.59–75.
[49]Parks DH,Tyson GW,Hugenholtz P,Beiko RG.STAMP:statistical analysis of taxonomic and functional profiles.Bioinformatics 2014;30:3123–4.