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Microscopic Methods for Identification of Sulfate-Reducing Bacteria From International Journal of Molecular Sciences Review Microscopic Methods for Identification of Sulfate-Reducing Bacteria from Various Habitats Ivan Kushkevych 1,* , Blanka Hýžová 1, Monika Vítˇezová 1 and Simon K.-M. R. Rittmann 2,* 1 Department of Experimental Biology, Faculty of Science, Masaryk University, 62500 Brno, Czech Republic; [email protected] (B.H.); [email protected] (M.V.) 2 Archaea Physiology & Biotechnology Group, Department of Functional and Evolutionary Ecology, Universität Wien, 1090 Wien, Austria * Correspondence: [email protected] (I.K.); [email protected] (S.K.-M.R.R.); Tel.: +420-549-495-315 (I.K.); +431-427-776-513 (S.K.-M.R.R.) Abstract: This paper is devoted to microscopic methods for the identification of sulfate-reducing bacteria (SRB). In this context, it describes various habitats, morphology and techniques used for the detection and identification of this very heterogeneous group of anaerobic microorganisms. SRB are present in almost every habitat on Earth, including freshwater and marine water, soils, sediments or animals. In the oil, water and gas industries, they can cause considerable economic losses due to their hydrogen sulfide production; in periodontal lesions and the colon of humans, they can cause health complications. Although the role of these bacteria in inflammatory bowel diseases is not entirely known yet, their presence is increased in patients and produced hydrogen sulfide has a cytotoxic effect. For these reasons, methods for the detection of these microorganisms were described. Apart from selected molecular techniques, including metagenomics, fluorescence microscopy was one of the applied methods. Especially fluorescence in situ hybridization (FISH) in various modifications Citation: Kushkevych, I.; Hýžová, B.; was described. This method enables visual identification of SRB, determining their abundance and Vítˇezová,M.; Rittmann, S.K.-M.R. Microscopic Methods for spatial distribution in environmental biofilms and gut samples. Identification of Sulfate-Reducing Bacteria from Various Habitats. Int. J. Keywords: microscopy; fluorescence microscopy; FISH; DAPI; Desulfovibrio; anaerobic microorganisms; Mol. Sci. 2021, 22, 4007. https:// habitats; SRB; SRP; SRM; sulfate reduction; identification; gut microbiota; IBD doi.org/10.3390/ijms22084007 Academic Editors: Márió Gajdács and Edit Urbán 1. Introduction Sulfate-reducing microorganisms (SRM) are a diverse group of anaerobic microorgan- Received: 26 February 2021 isms, which are widely present in nature and play an indispensable role in the sulfur and Accepted: 3 April 2021 carbon cycle on Earth [1]. This group comprises prokaryotes from the domains Bacteria and Published: 13 April 2021 Archaea, encompassing over 220 species from 60 different genera [2–4]. Members of this exceptional physiological group differ from each other in their nutritional requirements Publisher’s Note: MDPI stays neutral 2− and morphology; however, all its representatives use sulfate (SO4 ) or other oxidized with regard to jurisdictional claims in sulfur compounds as a terminal electron acceptor in the oxidation of organic substances [2]. published maps and institutional affil- As this review deals mainly with the representatives of the domain Bacteria, the term iations. sulfate-reducing bacteria (SRB) will be mainly used in the text. SRB can use a wide range of substances as electron donors. For example, molecular hydrogen (H2) and various organic compounds (lactate, acetate, pyruvate, malate, alcohols such as ethanol, propanol or butanol and others) can serve as electron donors in anaerobic Copyright: © 2021 by the authors. respiration [2,5]. Some SRB can also use nitrates as the final electron acceptor, for example, Licensee MDPI, Basel, Switzerland. the representatives of the genera Desulfovibrio or Desulfobacterium [6–9]. Organic substrates This article is an open access article can be oxidized by various species either incompletely to acetate (e.g., by the genus distributed under the terms and Desulfovibrio) or ultimately to carbon dioxide (e.g., by the genus Desulfomicrobium)[10]. conditions of the Creative Commons Attribution (CC BY) license (https:// The process is referred to as dissimilatory sulfate reduction or sulfate respiration. In this creativecommons.org/licenses/by/ process, a small amount of reduced sulfur is assimilated, but most of it is released into the 4.0/). Int. J. Mol. Sci. 2021, 22, 4007. https://doi.org/10.3390/ijms22084007 https://www.mdpi.com/journal/ijms Int. J. Mol. Sci. 2021, 22, x FOR PEER REVIEW 2 of 27 Int. J. Mol. Sci. 2021, 22, 4007 2 of 27 into the environment in the form of a sulfide ion, but usually as hydrogen sulfide (Figure 1). No other microorganisms than SRB are known to be capable of this form of respiration environment in the form of a sulfide ion, but usually as hydrogen sulfide (Figure1). No [11].other microorganisms than SRB are known to be capable of this form of respiration [11]. Figure 1. 1.Scheme Scheme of theof dissimilatorythe dissimilatory sulfate reduction.sulfate reduction. Intensive SRB studies started in 1895 when M. W. Beijerinck discovered an interesting biologicalIntensive activity SRB in a newlystudies isolated started species, in 1895 “Spirillum when desulfuricans M. W. Beijerinck” (later Desulfovibrio discovered an interest- ingdesulfuricans biological). Indeed, activity it was in the a dissimilatorynewly isolated sulfate species, reduction “ activitySpirillum that hedesulfuricans discovered. ” (later Desul- fovibrioMany other desulfuricans scientists went). Indeed, on to study it was SRB andthe new dissimilatory cultivation techniques sulfate reduction of anaerobes, activity that he discovered.and the development Many other of molecular scientists techniques went ledon toto thestudy characterization SRB and new of many cultivation new techniques taxa [2]. Recent studies are aiming to reveal the possible usage of SRB in biotechnology, oftoo, anaerobes, where SRB and can bethe used, development for example, of for molecular bioremediation techniques of toxic led compounds to the characterization in of manythe environment new taxa [12 [2].–15 Recent]. Other studies studies investigate are aiming SRB’s to reveal capability the to possible cause microbial usage of SRB in bio- technology,corrosion and oiltoo, acidification, where SRB which can is be causing used, considerable for example, economic for losses.bioremediation It is worth of toxic com- poundsmentioning in thatthe SRBenvironment inhabit very [12–15]. diverse habitats. Other studies These organisms investigate have SRB’s successfully capability to cause adapted to almost any ecosystem on Earth, from waters to soils and animal guts, humans microbialincluded. SRB corrosion were detected and oil in acidification, both the human whic intestinesh is causing and oral considerable cavity of patients economic losses. withIt is periodontitisworth mentioning [3]. Therefore, that anotherSRB inhabit important very field diverse of study habitats. considering Thes SRBe isorganisms their have suc- potentialcessfully role adapted in inflammatory to almost bowel any diseases ecosystem or periodontitis, on Earth, from as SRB waters produce to hydrogen soils and animal guts, humanssulfide, which included. is toxic toSRB cells were [15–20 detected]. The detail in informationboth the human regarding intestines the metabolism and oral of cavity of pa- SRB, their role in natural processes, or their industrial impacts can be found in the works tients with periodontitis [3]. Therefore, another important field of study considering SRB of R. Rabus, T.A Hansen and F. Widdel [21], J. M. Odom [22] or F. Widdel and F. Bak [23]. isConsidering their potential the wide role range in of inflammatory habitats in which SRBbowel can diseases be found, includingor periodontitis, their possible as SRB produce hydrogenimpact on human sulfide, health which and economics, is toxic to it cells is crucial [15–20]. to study The these detail microorganisms information further. regarding the me- Thetabolism mainpoints of SRB, that their should role be investigatedin natural processes, are the habitats or oftheir this industrial group of organisms, impacts can be found intheir the ecological works of interactions R. Rabus, and T.A finally, Hansen the development and F. Widdel of a broad[21], J. range M. Odom of efficient [22] or F. Widdel methods to reliably detect and identify them in the context of both research and clinical andusage. F. The Bak main [23]. points Considering that will be athe part wide of this range review of are habitats shown in in Figure which2. SRB can be found, in- cluding their possible impact on human health and economics, it is crucial to study these microorganisms further. The main points that should be investigated are the habitats of this group of organisms, their ecological interactions and finally, the development of a broad range of efficient methods to reliably detect and identify them in the context of both research and clinical usage. The main points that will be a part of this review are shown in Figure 2. Int. J. Mol. Sci. 2021, 22, x FOR PEER REVIEW 3 of 27 Int. J. Mol. Sci. 2021, 22, 4007 3 of 27 FigureFigure 2. 2.Main Main points points of the of review. the review. This review aims to describe the ecology and habitats of SRB, their morphology, which can beThis used review in detection aims via to microscopy, describe selected the ecolo moleculargy and methods habitats used toof identify SRB, their morphology, whichthis group, can and
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