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Understanding the Mechanisms of Positive Microbial Interactions That Benefit Lactic Acid Bacteria Co-Cultures

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Understanding the Mechanisms of Positive Microbial Interactions That Benefit Lactic Acid Bacteria Co-Cultures Understanding the Mechanisms of Positive Microbial Interactions That Benefit Lactic Acid Bacteria Co-cultures Fanny Canon, Thibault Nidelet, Eric Guédon, Anne Thierry, Valérie Gagnaire To cite this version: Fanny Canon, Thibault Nidelet, Eric Guédon, Anne Thierry, Valérie Gagnaire. Understanding the Mechanisms of Positive Microbial Interactions That Benefit Lactic Acid Bacteria Co-cultures. Fron- tiers in Microbiology, Frontiers Media, 2020, 11, 10.3389/fmicb.2020.02088. hal-02931021 HAL Id: hal-02931021 https://hal.archives-ouvertes.fr/hal-02931021 Submitted on 8 Jun 2021 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Distributed under a Creative Commons Attribution| 4.0 International License fmicb-11-02088 September 2, 2020 Time: 16:46 # 1 REVIEW published: 04 September 2020 doi: 10.3389/fmicb.2020.02088 Understanding the Mechanisms of Positive Microbial Interactions That Benefit Lactic Acid Bacteria Co-cultures Fanny Canon1, Thibault Nidelet2, Eric Guédon1, Anne Thierry1 and Valérie Gagnaire1* 1 STLO, INRAE, Institut Agro, Rennes, France, 2 SPO, INRAE, Montpellier SupAgro, Université de Montpellier, Montpellier, France Microorganisms grow in concert, both in natural communities and in artificial or synthetic co-cultures. Positive interactions between associated microbes are paramount to achieve improved substrate conversion and process performance in biotransformation and fermented food production. The mechanisms underlying such positive interactions have been the focus of numerous studies in recent decades and are now starting to be well characterized. Lactic acid bacteria (LAB) contribute to the final organoleptic, Edited by: nutritional, and health properties of fermented food products. However, interactions in Cristina Reguant, LAB co-cultures have been little studied, apart from the well-characterized LAB co- University of Rovira i Virgili, Spain culture used for yogurt manufacture. LAB are, however, multifunctional microorganisms Reviewed by: Giuseppe Spano, that display considerable potential to create positive interactions between them. This University of Foggia, Italy review describes why LAB co-cultures are of such interest, particularly in foods, and Pasquale Filannino, how their extensive nutritional requirements can be used to favor positive interactions. University of Bari Aldo Moro, Italy In that respect, our review highlights the benefits of co-cultures in different areas of *Correspondence: Valérie Gagnaire application, details the mechanisms underlying positive interactions and aims to show [email protected] how mechanisms based on nutritional interactions can be exploited to create efficient LAB co-cultures. Specialty section: This article was submitted to Keywords: positive interactions, co-culture, metabolic dependencies, lactic acid bacteria, cross-feeding, public Food Microbiology, goods, microbial community a section of the journal Frontiers in Microbiology Received: 12 May 2020 INTRODUCTION Accepted: 07 August 2020 Published: 04 September 2020 It is widely acknowledged that microorganisms have colonized most natural ecosystems and that Citation: no single strain grows in isolation, so that microbes are intertwined and constantly interacting. Canon F, Nidelet T, Guédon E, Scientists are now trying to understand the mechanisms underlying these interactions in order to Thierry A and Gagnaire V (2020) better control microbial communities and exploit them in a wide variety of bioprocesses. Understanding the Mechanisms Before detailing how microorganisms interact together, it is crucial to define the numerous of Positive Microbial Interactions That Benefit Lactic Acid Bacteria terms used in the literature which refer to their association, such as microbial community or Co-cultures. consortium, and mixed or co-cultures. As illustrated in Figure 1, we have chosen to use the term Front. Microbiol. 11:2088. natural community when referring to self-assembled communities of environmental microbes doi: 10.3389/fmicb.2020.02088 in various ecosystems (Rodríguez Amor and Dal Bello, 2019), and co-culture when referring to Frontiers in Microbiology| www.frontiersin.org 1 September 2020| Volume 11| Article 2088 fmicb-11-02088 September 2, 2020 Time: 16:46 # 2 Canon et al. Design of LAB Positive Interactions man-made associations of microorganisms (Zhang and Wang, characterized (Sieuwerts et al., 2008) and offers a perfect example 2016). We also use ‘assembly’ as an umbrella term which which asserts that LAB co-cultures are of value. encompasses both self-assembled communities and assembled The aim of this review is to highlight the optimum ways co-cultures. Biotechnological processes are reliant on three available at present that could be used to create positive types of assemblies: enriched natural communities, artificial co- interactions between LAB. We start with an overview of cultures and synthetic co-cultures (Figure 1). Here, artificial the different types of positive interactions in various existing co-cultures refer to cultures composed of microorganisms that microbial assemblies. We then address the added value of co- are generally not found together in nature, whereas synthetic cultivation and explain which mechanisms govern the positive co-cultures concern associations of microorganisms in which interactions encountered in microbial communities and co- at least one of the strains is a genetically modified organism cultures. Thirdly, we focus specifically on the possible strategies (GMO). Depending on the type of microbial assembly, the aim that could be used to assemble LAB. And finally, we highlight is (1) to increase or decrease concentrations in the targeted the particular role of nutritional interactions in LAB insofar as molecules, described as overyielding (Rapaport et al., 2020), by we consider their nutritional requirements to be the best lever to using the division of labor (DOL), or/and (2) to multiply the create positive interactions and new LAB co-cultures. functions expressed compared to monocultures. Regardless of the objectives, in each case the outcomes are reliant on positive interactions between the microorganisms that also enhance their POSITIVE INTERACTIONS IN fitness. For this reason, negative interactions, e.g., competition, CO-CULTURES: POTENTIAL cheating or parasitism, will not be covered in this review. USEFULNESS, TYPES AND Major efforts have been made to understand the mechanisms affecting the association of microorganisms in order to improve MECHANISMS process outputs. The need for direct contact (Zengler and Palsson, 2012), use of quorum sensing (QS) (Rul and Monnet, Microbial Communities and Co-cultures: 2015), environmental adjustments (Cheirsilp et al., 2003), the Purposes and Benefits sharing of public goods (Cavaliere et al., 2017) and cross- As the saying goes, there is strength in numbers, whether this feeding (D’Souza et al., 2018) have all been described during concerns microbial communities or man-made co-cultures. It is recent decades as possible ways to drive interactions among clear that natural transformations, for example the mineralization microbial communities. of organic matter in soils, can occur because microorganisms The value of co-cultivation has been exploited in many are able to grow in concert. Moreover, as stated by Ghosh et al. fields, from wastewater treatments based on enriched microbial (2016),“the application of co-culture in different bioprocesses can communities (Cydzik-Kwiatkowska and Zielinska´ , 2016) to be more advantageous than monocultures from the perspective the production of molecules of interest such as vitamin C of broader array of substrate utilization, coupled metabolic using artificial or/and synthetic co-cultures (Zou et al., 2013; performance and higher combined yield”. Thus, co-cultivation can Wang et al., 2016) or a huge number of fermented foods be used for two purposes: to enable substrate conversion and produced worldwide. Increasing microorganism fitness, product improve process performance (Figure 1). functionalities and the production of specific molecules is crucial We can distinguish two types of microbial assembly: self- in the area of food applications. For example, it has been shown assembled communities and assembled co-cultures. The first that co-cultures can enhance levels of peptides and amino acids gathers natural communities, enriched or not, which are (Gobbetti et al., 1994), organic acids (Settachaimongkon et al., spontaneous associations of microorganisms within a specific 2014) and volatile compounds (Álvarez-Martín et al., 2008) in biotope. They present the highest complexity in terms of the fermented foods, and contribute to more rapid microbial growth microbial species present and hence of the resulting interactions. when compared to monocultures (Stadie et al., 2013). The dynamics of natural communities are governed by natural Lactic acid bacteria (LAB) are ubiquitous in food fermentation selection. Evolution occurs in such a way that there is a constant and they have positive effects on the organoleptic, health, back and
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