Metatranscriptomics reveals temperature-driven functional changes in microbiome impacting cheese maturation rate

De Filippis, Francesca; Genovese, Alessandro; Ferranti, Pasquale; Gilbert, Jack A.; Ercolini, Danilo

doi:10.1038/srep21871

Metatranscriptomics reveals temperature-driven functional changes in microbiome impacting cheese maturation rate

Journal Article · Thu Feb 25 00:00:00 EST 2016 · Scientific Reports

DOI:https://doi.org/10.1038/srep21871· OSTI ID:1258637

De Filippis, Francesca ^[1]; Genovese, Alessandro ^[1]; Ferranti, Pasquale ^[1]; Gilbert, Jack A. ^[2]; Ercolini, Danilo ^[1]

Univ. of Naples Federico II (Italy)
Argonne National Lab. (ANL), Argonne, IL (United States); Univ. of Chicago, IL (United States)

Traditional cheeses harbour complex microbial consortia that play an important role in shaping typical sensorial properties. However, the microbial metabolism is considered difficult to control. Microbial community succession and the related gene expression were analysed during ripening of a traditional Italian cheese, identifying parameters that could be modified to accelerate ripening. Afterwards, we modulated ripening conditions and observed consistent changes in microbial community structure and function. We provide concrete evidence of the essential contribution of non-starter lactic acid bacteria in ripening-related activities. An increase in the ripening temperature promoted the expression of genes related to proteolysis, lipolysis and amino acid/lipid catabolism and significantly increases the cheese maturation rate. Moreover, temperature-promoted microbial metabolisms were consistent with the metabolomic profiles of proteins and volatile organic compounds in the cheese. Finally, the results clearly indicate how processing-driven microbiome responses can be modulated in order to optimize production efficiency and product quality.

View Accepted Manuscript (DOE)

Research Organization:: Argonne National Laboratory (ANL), Argonne, IL (United States)

Sponsoring Organization:: USDOE

OSTI ID:: 1258637

Journal Information:: Scientific Reports, Journal Name: Scientific Reports Vol. 6; ISSN 2045-2322

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

References (50)

Role of intestinal brush border peptidases in the simulated digestion of milk proteins Picariello, Gianluca; Miralles, Beatriz; Mamone, Gianfranco Molecular Nutrition & Food Research, Vol. 59, Issue 5 https://doi.org/10.1002/mnfr.201400856	journal	March 2015
Proteolytic systems of lactic acid bacteria Savijoki, Kirsi; Ingmer, Hanne; Varmanen, Pekka Applied Microbiology and Biotechnology, Vol. 71, Issue 4 https://doi.org/10.1007/s00253-006-0427-1	journal	April 2006
Cheese Rind Communities Provide Tractable Systems for In Situ and In Vitro Studies of Microbial Diversity Wolfe, Benjamin E.; Button, Julie E.; Santarelli, Marcela Cell, Vol. 158, Issue 2 https://doi.org/10.1016/j.cell.2014.05.041	journal	July 2014
Fermented Foods as Experimentally Tractable Microbial Ecosystems Wolfe, Benjamin E.; Dutton, Rachel J. Cell, Vol. 161, Issue 1 https://doi.org/10.1016/j.cell.2015.02.034	journal	March 2015
Assessing the proteolytic and lipolytic activities of single strains of mesophilic lactobacilli as adjunct cultures using a Caciotta cheese model system Di Cagno, Raffaella; Quinto, Maurizio; Corsetti, Aldo International Dairy Journal, Vol. 16, Issue 2 https://doi.org/10.1016/j.idairyj.2005.01.012	journal	February 2006
The effect of Lactobacillus buchneri and Lactobacillus parabuchneri on the eye formation of semi-hard cheese Fröhlich-Wyder, Marie-Therese; Guggisberg, Dominik; Badertscher, René International Dairy Journal, Vol. 33, Issue 2 https://doi.org/10.1016/j.idairyj.2013.03.004	journal	December 2013
Traditional cheeses: Rich and diverse microbiota with associated benefits Montel, Marie-Christine; Buchin, Solange; Mallet, Adrien International Journal of Food Microbiology, Vol. 177 https://doi.org/10.1016/j.ijfoodmicro.2014.02.019	journal	May 2014
Optimization of Solid Phase Microextraction Analysis for the Headspace Volatile Compounds of Parmesan Cheese Lee, Jae-Hwan; Diono, Raymond; Kim, Gur-Yoo Journal of Agricultural and Food Chemistry, Vol. 51, Issue 5 https://doi.org/10.1021/jf025910+	journal	January 2003
Multifactorial diversity sustains microbial community stability Erkus, Oylum; de Jager, Victor CL; Spus, Maciej The ISME Journal, Vol. 7, Issue 11 https://doi.org/10.1038/ismej.2013.108	journal	July 2013
QIIME allows analysis of high-throughput community sequencing data Caporaso, J. Gregory; Kuczynski, Justin; Stombaugh, Jesse Nature Methods, Vol. 7, Issue 5 https://doi.org/10.1038/nmeth.f.303	journal	April 2010
The Sequence Alignment/Map format and SAMtools Li, H.; Handsaker, B.; Wysoker, A. Bioinformatics, Vol. 25, Issue 16 https://doi.org/10.1093/bioinformatics/btp352	journal	June 2009
Search and clustering orders of magnitude faster than BLAST Edgar, Robert C. Bioinformatics, Vol. 26, Issue 19, p. 2460-2461 https://doi.org/10.1093/bioinformatics/btq461	journal	August 2010
Data, information, knowledge and principle: back to metabolism in KEGG Kanehisa, Minoru; Goto, Susumu; Sato, Yoko Nucleic Acids Research, Vol. 42, Issue D1 https://doi.org/10.1093/nar/gkt1076	journal	November 2013
Cytoscape: A Software Environment for Integrated Models of Biomolecular Interaction Networks Shannon, P. Genome Research, Vol. 13, Issue 11 https://doi.org/10.1101/gr.1239303	journal	November 2003
Naive Bayesian Classifier for Rapid Assignment of rRNA Sequences into the New Bacterial Taxonomy Wang, Q.; Garrity, G. M.; Tiedje, J. M. Applied and Environmental Microbiology, Vol. 73, Issue 16 https://doi.org/10.1128/aem.00062-07	journal	June 2007
Microbial Ecology Dynamics Reveal a Succession in the Core Microbiota Involved in the Ripening of Pasta Filata Caciocavallo Pugliese Cheese De Pasquale, Ilaria; Di Cagno, Raffaella; Buchin, Solange Applied and Environmental Microbiology, Vol. 80, Issue 19 https://doi.org/10.1128/aem.02097-14	journal	August 2014
“Remake” by High-Throughput Sequencing of the Microbiota Involved in the Production of Water Buffalo Mozzarella Cheese Ercolini, Danilo; De Filippis, Francesca; La Storia, Antonietta Applied and Environmental Microbiology, Vol. 78, Issue 22 https://doi.org/10.1128/aem.02218-12	journal	August 2012
Temporal and Spatial Differences in Microbial Composition during the Manufacture of a Continental-Type Cheese O'Sullivan, Daniel J.; Cotter, Paul D.; O'Sullivan, Orla Applied and Environmental Microbiology, Vol. 81, Issue 7 https://doi.org/10.1128/aem.04054-14	journal	January 2015
SolexaQA: At-a-glance quality assessment of Illumina second-generation sequencing data Cox, Murray P.; Peterson, Daniel A.; Biggs, Patrick J. BMC Bioinformatics, Vol. 11, Issue 1 https://doi.org/10.1186/1471-2105-11-485	journal	September 2010
The proteolytic system of lactic acid bacteria revisited: a genomic comparison Liu, Mengjin; Bayjanov, Jumamurat R.; Renckens, Bernadet BMC Genomics, Vol. 11, Issue 1 https://doi.org/10.1186/1471-2164-11-36	journal	January 2010
Metatranscriptome analysis of fungal strains Penicillium camemberti and Geotrichum candidum reveal cheese matrix breakdown and potential development of sensory properties of ripened Camembert-type cheese Lessard, Marie-Hélène; Viel, Catherine; Boyle, Brian BMC Genomics, Vol. 15, Issue 1 https://doi.org/10.1186/1471-2164-15-235	journal	January 2014
Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2 Love, Michael I.; Huber, Wolfgang; Anders, Simon Genome Biology, Vol. 15, Issue 12 https://doi.org/10.1186/s13059-014-0550-8	journal	December 2014
A Selected Core Microbiome Drives the Early Stages of Three Popular Italian Cheese Manufactures De Filippis, Francesca; La Storia, Antonietta; Stellato, Giuseppina PLoS ONE, Vol. 9, Issue 2 https://doi.org/10.1371/journal.pone.0089680	journal	February 2014
The Same Microbiota and a Potentially Discriminant Metabolome in the Saliva of Omnivore, Ovo-Lacto-Vegetarian and Vegan Individuals De Filippis, Francesca; Vannini, Lucia; La Storia, Antonietta PLoS ONE, Vol. 9, Issue 11 https://doi.org/10.1371/journal.pone.0112373	journal	November 2014
Overview of a Surface-Ripened Cheese Community Functioning by Meta-Omics Analyses Dugat-Bony, Eric; Straub, Cécile; Teissandier, Aurélie PLOS ONE, Vol. 10, Issue 4 https://doi.org/10.1371/journal.pone.0124360	journal	April 2015
Relationships Between Flavoring Capabilities, Bacterial Composition, and Geographical Origin of Natural Whey Cultures Used for Traditional Water-Buffalo Mozzarella Cheese Manufacture Mauriello, G.; Moio, L.; Genovese, A. Journal of Dairy Science, Vol. 86, Issue 2 https://doi.org/10.3168/jds.s0022-0302(03)73627-3	journal	February 2003
Nucleic acid-based approaches to investigate microbial-related cheese quality defects O'Sullivan, Daniel J.; Giblin, Linda; McSweeney, Paul L. H. Frontiers in Microbiology, Vol. 4 https://doi.org/10.3389/fmicb.2013.00001	journal	January 2013
mBLAST: Keeping up with the Sequencing Explosion for (Meta) Genome Analysis Davis, Curtis Journal of Data Mining in Genomics & Proteomics, Vol. 04, Issue 03 https://doi.org/10.4172/2153-0602.1000135	journal	January 2013
Characterization of the volatile organic compounds of Italian ‘Fossa’ cheese by solid-phase microextraction gas chromatography/mass spectrometry Gioacchini, Anna Maria; De Santi, Mauro; Guescini, Michele Rapid Communications in Mass Spectrometry, Vol. 24, Issue 23 https://doi.org/10.1002/rcm.4782	journal	November 2010
A peptidomic approach for monitoring and characterising peptide cyanotoxins produced in Italian lakes by matrix-assisted laser desorption/ionisation and quadrupole time-of-flight mass spectrometry: Profiling cyanotoxins in Italian lakes by mass spectrometry Ferranti, Pasquale; Nasi, Antonella; Bruno, Milena Rapid Communications in Mass Spectrometry, Vol. 25, Issue 9 https://doi.org/10.1002/rcm.4973	journal	April 2011
Proteolytic enzymes of lactic acid bacteria Law, Jean; Haandrikman, Alfred International Dairy Journal, Vol. 7, Issue 1 https://doi.org/10.1016/0958-6946(95)00073-9	journal	January 1997
Flavours of cheese products: metabolic pathways, analytical tools and identification of producing strains Marilley, L. International Journal of Food Microbiology, Vol. 90, Issue 2 https://doi.org/10.1016/S0168-1605(03)00304-0	journal	January 2004
Microbiological, compositional, biochemical and textural characterisation of Caciocavallo Pugliese cheese during ripening Gobbetti, M.; Morea, M.; Baruzzi, F. International Dairy Journal, Vol. 12, Issue 6 https://doi.org/10.1016/S0958-6946(02)00042-0	journal	January 2002
Zooming into food-associated microbial consortia: a ‘cultural’ evolution Cocolin, Luca; Ercolini, Danilo Current Opinion in Food Science, Vol. 2 https://doi.org/10.1016/j.cofs.2015.01.003	journal	April 2015
Flavour formation by lactic acid bacteria and biochemical flavour profiling of cheese products Smit, Gerrit; Smit, Bart A.; Engels, Wim J. M. FEMS Microbiology Reviews, Vol. 29, Issue 3 https://doi.org/10.1016/j.fmrre.2005.04.002	journal	August 2005
Monocarboxylic acid production by lactococci and lactobacilli Ganesan, Balasubramanian; Seefeldt, Kimberly; Koka, Ramarathna C. International Dairy Journal, Vol. 14, Issue 3 https://doi.org/10.1016/j.idairyj.2003.07.004	journal	March 2004
Discrimination of commercial Caciocavallo cheeses on the basis of the diversity of lactic microflora and primary proteolysis Piraino, Paolo; Zotta, Teresa; Ricciardi, Annamaria International Dairy Journal, Vol. 15, Issue 11 https://doi.org/10.1016/j.idairyj.2004.12.006	journal	November 2005
Contribution of autochthonous non-starter lactobacilli to proteolysis in Caciocavallo Pugliese cheese Morea, M.; Matarante, A.; Di Cagno, R. International Dairy Journal, Vol. 17, Issue 5 https://doi.org/10.1016/j.idairyj.2006.05.010	journal	May 2007
Microbial diversity in Natural Whey Cultures used for the production of Caciocavallo Silano PDO cheese Ercolini, D.; Frisso, G.; Mauriello, G. International Journal of Food Microbiology, Vol. 124, Issue 2 https://doi.org/10.1016/j.ijfoodmicro.2008.03.007	journal	May 2008
An improved Greengenes taxonomy with explicit ranks for ecological and evolutionary analyses of bacteria and archaea McDonald, Daniel; Price, Morgan N.; Goodrich, Julia The ISME Journal, Vol. 6, Issue 3 https://doi.org/10.1038/ismej.2011.139	journal	December 2011
Fast gapped-read alignment with Bowtie 2 Langmead, Ben; Salzberg, Steven L. Nature Methods, Vol. 9, Issue 4 https://doi.org/10.1038/nmeth.1923	journal	March 2012
Survey of lactic acid bacteria during the ripening of Caciocavallo cheese produced in Molise Coppola, Raffaele; Succi, Mariantonietta; Sorrentino, Elena Le Lait, Vol. 83, Issue 3 https://doi.org/10.1051/lait:2003011	journal	May 2003
Naive Bayesian Classifier for Rapid Assignment of rRNA Sequences into the New Bacterial Taxonomy Wang, Q.; Garrity, G. M.; Tiedje, J. M. Applied and Environmental Microbiology, Vol. 73, Issue 16 https://doi.org/10.1128/AEM.00062-07	journal	June 2007
Microbial Ecology Dynamics Reveal a Succession in the Core Microbiota Involved in the Ripening of Pasta Filata Caciocavallo Pugliese Cheese De Pasquale, Ilaria; Di Cagno, Raffaella; Buchin, Solange Applied and Environmental Microbiology, Vol. 80, Issue 19 https://doi.org/10.1128/AEM.02097-14	journal	August 2014
“Remake” by High-Throughput Sequencing of the Microbiota Involved in the Production of Water Buffalo Mozzarella Cheese Ercolini, Danilo; De Filippis, Francesca; La Storia, Antonietta Applied and Environmental Microbiology, Vol. 78, Issue 22 https://doi.org/10.1128/AEM.02218-12	journal	August 2012
Temporal and Spatial Differences in Microbial Composition during the Manufacture of a Continental-Type Cheese O'Sullivan, Daniel J.; Cotter, Paul D.; O'Sullivan, Orla Applied and Environmental Microbiology, Vol. 81, Issue 7 https://doi.org/10.1128/AEM.04054-14	journal	January 2015
Cutadapt removes adapter sequences from high-throughput sequencing reads Martin, Marcel EMBnet.journal, Vol. 17, Issue 1 https://doi.org/10.14806/ej.17.1.200	journal	May 2011
Improving the flavour of cheese Weimer, Bart C. https://doi.org/10.1533/9781845693053	book	January 2007
Accelerated ripening of Caciocavallo Pugliese cheese with attenuated adjuncts of selected nonstarter lactobacilli Di Cagno, R.; De Pasquale, I.; De Angelis, M. Journal of Dairy Science, Vol. 95, Issue 9 https://doi.org/10.3168/jds.2011-5283	journal	September 2012
Relationships Between Flavoring Capabilities, Bacterial Composition, and Geographical Origin of Natural Whey Cultures Used for Traditional Water-Buffalo Mozzarella Cheese Manufacture Mauriello, G.; Moio, L.; Genovese, A. Journal of Dairy Science, Vol. 86, Issue 2 https://doi.org/10.3168/jds.S0022-0302(03)73627-3	journal	February 2003

Cited By (17)

Pan-genomic and transcriptomic analyses of Leuconostoc mesenteroides provide insights into its genomic and metabolic features and roles in kimchi fermentation Chun, Byung Hee; Kim, Kyung Hyun; Jeon, Hye Hee Scientific Reports, Vol. 7, Issue 1 https://doi.org/10.1038/s41598-017-12016-z	journal	September 2017
Cream Cheese-Derived Lactococcus chungangensis CAU 28 Modulates the Gut Microbiota and Alleviates Atopic Dermatitis in BALB/c Mice Kim, Jong-Hwa; Kim, Kiyoung; Kim, Wonyong Scientific Reports, Vol. 9, Issue 1 https://doi.org/10.1038/s41598-018-36864-5	journal	January 2019
Metagenomics insights into food fermentations De Filippis, Francesca; Parente, Eugenio; Ercolini, Danilo Microbial Biotechnology, Vol. 10, Issue 1 https://doi.org/10.1111/1751-7915.12421	journal	October 2016
Carrot Juice Fermentations as Man-Made Microbial Ecosystems Dominated by Lactic Acid Bacteria Wuyts, Sander; Van Beeck, Wannes; Oerlemans, Eline F. M. Applied and Environmental Microbiology, Vol. 84, Issue 12 https://doi.org/10.1128/aem.00134-18	journal	April 2018
High Throughput Sequencing Technologies as a New Toolbox for Deep Analysis, Characterization and Potentially Authentication of Protection Designation of Origin Cheeses? Kamilari, Elena; Tomazou, Marios; Antoniades, Athos International Journal of Food Science, Vol. 2019 https://doi.org/10.1155/2019/5837301	journal	November 2019
Unraveling Core Functional Microbiota in Traditional Solid-State Fermentation by High-Throughput Amplicons and Metatranscriptomics Sequencing Song, Zhewei; Du, Hai; Zhang, Yan Frontiers in Microbiology, Vol. 8 https://doi.org/10.3389/fmicb.2017.01294	journal	July 2017
A Review on the Applications of Next Generation Sequencing Technologies as Applied to Food-Related Microbiome Studies Cao, Yu; Fanning, Séamus; Proos, Sinéad Frontiers in Microbiology, Vol. 8 https://doi.org/10.3389/fmicb.2017.01829	journal	September 2017
Sequencing of the Cheese Microbiome and Its Relevance to Industry Yeluri Jonnala, Bhagya. R.; McSweeney, Paul L. H.; Sheehan, Jeremiah J. Frontiers in Microbiology, Vol. 9 https://doi.org/10.3389/fmicb.2018.01020	journal	May 2018
Systems Biology – A Guide for Understanding and Developing Improved Strains of Lactic Acid Bacteria Liu, Jianming; Chan, Siu Hung Joshua; Chen, Jun Frontiers in Microbiology, Vol. 10 https://doi.org/10.3389/fmicb.2019.00876	journal	April 2019
Raw Material Regulates Flavor Formation via Driving Microbiota in Chinese Liquor Fermentation Liu, Chongchong; Feng, Shengbao; Wu, Qun Frontiers in Microbiology, Vol. 10 https://doi.org/10.3389/fmicb.2019.01520	journal	July 2019
Transcription Profiling Reveals Cooperative Metabolic Interactions in a Microbial Cheese-Ripening Community Composed of Debaryomyces hansenii, Brevibacterium aurantiacum, and Hafnia alvei Pham, Nguyen-Phuong; Landaud, Sophie; Lieben, Pascale Frontiers in Microbiology, Vol. 10 https://doi.org/10.3389/fmicb.2019.01901	journal	August 2019
Capturing the genetic makeup of the active microbiome in situ Singer, Esther; Wagner, Michael; Woyke, Tanja The ISME Journal, Vol. 11, Issue 9 https://doi.org/10.1038/ismej.2017.59	journal	June 2017
Consistent microbial dynamics and functional community patterns derived from first principles Delattre, Hadrien; Desmond-Le Quéméner, Elie; Duquennoi, Christian The ISME Journal, Vol. 13, Issue 2 https://doi.org/10.1038/s41396-018-0272-0	journal	September 2018
Cheesomics: the future pathway to understanding cheese flavour and quality Afshari, Roya; Pillidge, Christopher J.; Dias, Daniel A. Critical Reviews in Food Science and Nutrition, Vol. 60, Issue 1 https://doi.org/10.1080/10408398.2018.1512471	journal	October 2018
Metagenome-based surveillance and diagnostic approaches to studying the microbial ecology of food production and processing environments: Metagenome-based surveillance and diagnostic approaches Doyle, Conor J.; O'Toole, Paul W.; Cotter, Paul D. Environmental Microbiology, Vol. 19, Issue 11 https://doi.org/10.1111/1462-2920.13859	journal	September 2017
Microbiota of an Italian Grana-Like Cheese during Manufacture and Ripening, Unraveled by 16S rRNA-Based Approaches Alessandria, Valentina; Ferrocino, Ilario; De Filippis, Francesca Applied and Environmental Microbiology, Vol. 82, Issue 13 https://doi.org/10.1128/aem.00999-16	journal	April 2016
How to normalize metatranscriptomic count data for differential expression analysis Klingenberg, Heiner; Meinicke, Peter PeerJ, Vol. 5 https://doi.org/10.7717/peerj.3859	journal	January 2017

Similar Records

Quality of goat′s milk cheese as affected by coating with edible chitosan‐essential oil films

Journal Article · Thu Aug 25 20:00:00 EDT 2016 · International Journal of Dairy Technology · OSTI ID:1401227

Metatranscriptomics and Amplicon Sequencing Reveal Mutualisms in Seagrass Microbiomes

Journal Article · Wed Mar 14 20:00:00 EDT 2018 · Frontiers in Microbiology · OSTI ID:1628164

Bioconversion of Cheese Waste (Whey)

Technical Report · Tue Mar 10 23:00:00 EST 1998 · OSTI ID:16549

Related Subjects

60 APPLIED LIFE SCIENCES

Metatranscriptomics reveals temperature-driven functional changes in microbiome impacting cheese maturation rate

Citation Formats

References (50)

Cited By (17)

Similar Records

Related Subjects