Effects of sub-lethal high-pressure homogenization treatment on the outermost cellular structures and the volatile-molecule profiles of two strains of probiotic lactobacilli

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Abstract

Applying sub-lethal levels of high-pressure homogenization (HPH) to lactic acid bacteria has been proposed as a method of enhancing some of their functional properties. Because the principal targets of HPH are the cell-surface structures, the aim of this study was to examine the effect of sub-lethal HPH treatment on the outermost cellular structures and the proteomic profiles of two known probiotic bacterial strains. Moreover, the effect of HPH treatment on the metabolism of probiotic cells within a dairy product during its refrigerated storage was investigated using SPME-GC-MS. Transmission electron microscopy was used to examine the microstructural changes in the outermost cellular structures due to HPH treatment. These alterations may be involved in the changes in some of the technological and functional properties of the strains that were observed after pressure treatment. Moreover, the proteomic profiles of the probiotic strains treated with HPH and incubated at 37°C for various periods showed different peptide patterns compared with those of the untreated cells. In addition, there were differences in the peaks that were observed in the low-mass spectral region (2000–3000 Da) of the spectral profiles of the control and treated samples. Due to pressure treatment, the volatile-molecule profiles of buttermilk inoculated with treated or control cells and stored at 4°C for 30 days exhibited overall changes in the aroma profile and in the production of molecules that improved its sensory profile, although the two different species imparted specific fingerprints to the product. The results of this study will contribute to understanding the changes that occur in the outermost cellular structures and the metabolism of LAB in response to HPH treatment. The findings of this investigation may contribute to elucidating the relationships between these changes and the alterations of the technological and functional properties of LAB induced by pressure treatment.

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Most cited references 37

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Functional analysis of putative adhesion factors in Lactobacillus acidophilus NCFM.

B. Logan Buck, Eric Altermann, Tina Svingerud … (2005)

Lactobacilli are major inhabitants of the normal microflora of the gastrointestinal tract, and some select species have been used extensively as probiotic cultures. One potentially important property of these organisms is their ability to interact with epithelial cells in the intestinal tract, which may promote retention and host-bacterial communication. However, the mechanisms by which they attach to intestinal epithelial cells are unknown. The objective of this study was to investigate cell surface proteins in Lactobacillus acidophilus that may promote attachment to intestinal tissues. Using genome sequence data, predicted open reading frames were searched against known protein and protein motif databases to identify four proteins potentially involved in adhesion to epithelial cells. Homologous recombination was used to construct isogenic mutations in genes encoding a mucin-binding protein, a fibronectin-binding protein, a surface layer protein, and two streptococcal R28 homologs. The abilities of the mutants to adhere to intestinal epithelial cells were then evaluated in vitro. Each strain was screened on Caco-2 cells, which differentiate and express markers characteristic of normal small-intestine cells. A significant decrease in adhesion was observed in the fibronectin-binding protein mutant (76%) and the mucin-binding protein mutant (65%). A surface layer protein mutant also showed reduction in adhesion ability (84%), but the effect of this mutation is likely due to the loss of multiple surface proteins that may be embedded in the S-layer. This study demonstrated that multiple cell surface proteins in L. acidophilus NCFM can individually contribute to the organism's ability to attach to intestinal cells in vitro.

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The influence of polyunsaturated fatty acids on probiotic growth and adhesion.

Marietta Y. W. T. Lee, E Isolauri, Tiina S. Salminen … (2001)

The establishment of the intestinal microflora, and probiotic bacteria, may control the inflammatory conditions in the gut. As polyunsaturated fatty acids (PUFA) possess antimicrobial activities, they may deter the action of probiotics. We assessed whether free linoleic, gamma-linolenic, arachidonic, alpha-linolenic and docosahexaenoic acids at physiological concentrations in the growth media would influence the growth and adhesion of Lactobacillus GG (probiotic), Lactobacillus casei Shirota (probiotic) and Lactobacillus bulgaricus (dairy strain). Higher concentrations of PUFA (10-40 microg PUFA ml(-1)) inhibited growth and mucus adhesion of all tested bacterial strains, whilst growth and mucus adhesion of L. casei Shirota was promoted by low concentrations of gamma-linolenic acid and arachidonic acid (at 5 microg ml(-1)), respectively. PUFA also altered bacterial adhesion sites on Caco-2 cells. Caco-2 cells grown in the presence of arachidonic acid were less adhered to by all three bacterial strains. Yet, L. casei Shirota adhered better on Caco-2 cells grown in the presence of alpha-linolenic acid. As the adhesion to mucosal surfaces is pivotal in health promoting effects by probiotics, our results indicate that the action of probiotics in the gut may be modulated by dietary PUFA.

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Viability of probiotic (Bifidobacterium, Lactobacillus acidophilus and Lactobacillus casei) and nonprobiotic microflora in Argentinian Fresco cheese.

C G Vinderola, W Prosello, T D Ghiberto … (2000)

We evaluated the suitability of Argentinian Fresco cheese as a food carrier of probiotic cultures. We used cultures of Bifidobacterium bifidum (two strains), Bifidobacterium longum (two strains), Bifidobacterium sp. (one strain), Lactobacillus acidophilus (two strains), and Lactobacillus casei (two strains) in different combinations, as probiotic adjuncts. Probiotic, lactic starter (Lactococcus lactis and Streptococcus thermophilus), and contaminant (coliforms, yeasts, and molds) organisms were counted at 0, 30, and 60 d of refrigerated storage. Furthermore, the acid resistance of probiotic and starter bacteria was determined from hydrochloric solutions (pH 2 and 3) of Fresco cheese. The results showed that nine different combinations of bifidobacteria and L. acidophilus had a satisfactory viability (count decreases in 60 d <1 log order) in the cheese. Both combinations of bifidobacteria and L. casei cultures assayed also showed a satisfactory survival (counts decreased <1 log order for bifidobacteria but no decrease was detected for L. casei). On the other hand, the three combinations of bifidobacteria, L. acidophilus, and L. casei tested adapted well to the Fresco cheese environment. When a cheese homogenate at pH 3 was used to partially simulate the acidic conditions in the stomach, the probiotic cultures had an excellent ability to remain viable up to 3 h. At pH 2, the cell viability was more affected; B. bifidum was the most resistant organism. This study showed that the Argentinian Fresco cheese could be used as an adequate carrier of probiotic bacteria.

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Author and article information

Contributors

Giulia Tabanelli: URI : http://loop.frontiersin.org/people/213306/overview

Pamela Vernocchi: URI : http://loop.frontiersin.org/people/74808/overview

Francesca Patrignani: URI : http://loop.frontiersin.org/people/213332/overview

Federica Del Chierico: URI : http://loop.frontiersin.org/people/74809/overview

Lorenza Putignani: URI : http://loop.frontiersin.org/people/21900/overview

Gabriel Vinderola: URI : http://loop.frontiersin.org/people/22997/overview

Jorge A. Reinheimer: URI : http://loop.frontiersin.org/people/18035/overview

Fausto Gardini: URI : http://loop.frontiersin.org/people/212680/overview

Rosalba Lanciotti: URI : http://loop.frontiersin.org/people/184311/overview

Journal

Journal ID (nlm-ta): Front Microbiol

Journal ID (iso-abbrev): Front Microbiol

Journal ID (publisher-id): Front. Microbiol.

Title: Frontiers in Microbiology

Publisher: Frontiers Media S.A.

ISSN (Electronic): 1664-302X

Publication date (Electronic): 23 September 2015

Publication date Collection: 2015

Volume: 6

Electronic Location Identifier: 1006

Affiliations

[1] ¹Centro Interdipartimentale di Ricerca Industriale Agroalimentare, Università degli Studi di Bologna Cesena, Italy

[2] ²Unit of Metagenomics, Bambino Gesù Children's Hospital, IRCCS Rome, Italy

[3] ³Dipartimento di Scienze e Tecnologie Agro-alimentari, Università degli Studi di Bologna – Sede di Cesena Cesena, Italy

[4] ⁴Unit of Parasitology, Bambino Gesù Children's Hospital, IRCCS Rome, Italy

[5] ⁵Facultad de Ingeniería Química, Instituto de Lactología Industrial (INLAIN, UNL-CONICET), Universidad Nacional del Litoral Santa Fe, Argentina

Author notes

Edited by: Javier Carballo, University of Vigo, Spain

Reviewed by: Maria Guadalupe Vizoso Pinto, National Univeristy of Tucumán, Argentina; Qingping Zhong, South China Agricultural University, China

*Correspondence: Rosalba Lanciotti, Dipartimento di Scienze e Tecnologie Agro-alimentari, Università degli Studi di Bologna – Sede di Cesena - Piazza Goidanich 60, 47521 Cesena, Italy rosalba.lanciotti@ 123456unibo.it

This article was submitted to Food Microbiology, a section of the journal Frontiers in Microbiology

Article

DOI: 10.3389/fmicb.2015.01006

PMC ID: 4585067

SO-VID: bc508f23-2934-4438-b22a-4a08e11a8f6e

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This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

History

Date received : 11 March 2015

Date accepted : 07 September 2015

Page count

Figures: 5, Tables: 3, Equations: 0, References: 39, Pages: 13, Words: 9110

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Effects of sub-lethal high-pressure homogenization treatment on the outermost cellular structures and the volatile-molecule profiles of two strains of probiotic lactobacilli

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Most cited references 37

Functional analysis of putative adhesion factors in Lactobacillus acidophilus NCFM.

The influence of polyunsaturated fatty acids on probiotic growth and adhesion.

Viability of probiotic (Bifidobacterium, Lactobacillus acidophilus and Lactobacillus casei) and nonprobiotic microflora in Argentinian Fresco cheese.

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