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Microbial Organic Compounds Generating Taste and Odor in Water

  • Dharumadurai Dhanasekaran
  • Saravanan Chandraleka
  • Govindhan Sivaranjani
  • Selvanathan Latha
Chapter
  • 340 Downloads
Part of the Environmental Chemistry for a Sustainable World book series (ECSW, volume 22)

Abstract

Odor compounds are mainly due to the presence of many volatile and semivolatile components with diverse chemical and physicochemical properties. These compounds are generally present within complex matrices. Odorous compounds in the soil have been subjected to scientific analysis for the determination of odor compounds produced by microorganisms. These compounds are also known as volatile organic compounds (VOCs). They are present in natural sources such as soil, air, freshwater, and marine water ecosystems, and they produce unpleasant musty odors or earthy odors.

VOCs have been isolated from Actinobacteria species, and these compounds play main roles in biological function. Common VOCs are alkanes, alkenes, alcohols, esters, ketones, sulfur compounds, and isoprenoid compounds. Geosmin and 2-methyl-isoborneol are naturally occurring compounds that have a very strong earthy taste and odor, and they can be simply detected by the human nose. Little is known about the fundamentals of microbial volatile odor compounds that contribute undesirable tastes or odors in water, soil, and aquaculture products. To address this knowledge gap, we have investigated the microbial community causing undesirable odors and tastes in water. The present review describes the microbial origin of odor compounds, particularly those caused by Actinobacteria. It also describes their distribution, occurrence, and chemical nature; detection of odor compounds; and biological methods used to remove undesirable odors from water.

Keywords

Streptomyces Odor compounds Geosmin Water odor and taste 

8.1 Introduction to Taste and Odor Problems

Taste and odor problems cause common concerns about water quality for water utilities (Lalezary et al. 1986) and are relevant to the consistency and safety of drinking water. Mostly, taste and odor problems pose no risks to human health, but they raise consumer concerns regarding water safety. However, these problems are easy to remedy through control of dosage or filtration. Many volatile organic compounds (VOCs) causing odor problems can be identified from Actinobacteria cultures. In some investigations, the presence of odorous compounds from actinobacterial metabolites has coincided with the observation of aerial mycelium and spores (Bentley and Meganathan 1981). The most prevalent of such consumer complaints involve earthy–musty odors, which are primarily the result of two odor-causing compounds—geosmin (trans-1,10-dimethyl-trans-9 decalol; C12H22O) and 2-methyl-isoborneol (C11H20O)—in drinking water obtained from surface water sources. Removal of geosmin and 2-methyl-isoborneol is challenging because of their low odor threshold. Although taste- and odor-causing compounds do not cause health problems, their persistence causes a negative impression that the water is unsafe. In view of such aesthetic water quality concerns, more research is required to verify their abundance and capability to be metabolically active in several locations in India and other countries. Little is known about the fundamentals of microbial volatile odor compounds that contribute tastes or undesirable odors to water, soil, and aquaculture products. To address this knowledge gap, we have investigated microbial communities causing undesirable odors and tastes in water. The present review describes the microbial origin of odor compounds, particularly from Actinobacteria; their distribution, occurrence, and chemical nature; methods for detection of odors in water, soil sediments, and aquaculture; and odor removal methods with biological treatments involving biofiltration, activated carbon, and advanced oxidation processing (AOP).

8.2 Principles of Odor Compounds

Natural odor compounds are found in soil, water, and certain specific exotic plant species. An attractive alternative method for flavor and fragrance synthesis is based on de novo microbial processes (fermentation) or bioconversion of natural precursors, using microbial cells and enzymes (biocatalysis). For the past 60 years it has been well known that microorganisms produce odor and taste chemicals. The characteristic flavor of any compound is mainly due to the presence of many volatile and nonvolatile components with diverse chemical and physicochemical properties. These compounds are generally present within complex matrices. Actinobacteria, particularly Streptomyces species are the main producers of odor compounds specifically 2-methyl-isoborneol and geosmin. However, different Streptomyces species have different abilities to produce 2-methyl-isoborneol and geosmin; therefore, some species may produce more odorous compounds than others.

8.3 Characteristics of Taste and Odor Compounds

The terms “taste” and “odor” are used jointly in the vernacular of water technology. As mentioned earlier, taste and odor problems in water supplies are concerned almost entirely with odors. Occurrences of tastes and odors at a water plant or in a water system are generally unpredictable. The odors caused by dead organic matter can be classified as vegetable odors and odors of decomposition. These smells vary in character in different waters and in different seasons.

Volatile compounds are easily transported through the air and, in most cases, dissemination of VOCs from their point of origin leads to atmospheric dilution of the substances (Bennett and Inamdar 2015). Approximately 1000 microbial VOCs have been identified to date (Piechulla and Degenhardt 2014). Bacterial VOCs also contribute to the ability of bacteria to interact with their environment. Indeed, several volatile compounds have been shown to influence growth, differentiation, stress resistance, and/or behavior in fungi, plants, or invertebrates (Wenke et al. 2012; Davis et al. 2013). Beyond such interactions with a wide range of eukaryote organisms, recent studies have revealed the roles of odor compounds in bacterial interactions in various environments, including soil, animal and plant microbiota, and biofilms. Geosmin, as mentioned earlier, is an odor-producing compound produced by certain species of Actinobacteria in water. Actinobacteria-derived taste and odor compounds are listed in Table 8.1.
Table 8.1

Taste and odor description, chemical nature, and structure of earthy, woody, musty, and moldy odor–causing volatile organic compounds (VOCs) derived from the actinobacterial genera Actinomadura, Micromonospora, Nocardioides, and Streptomyces

Taste and odor description

Bacteria

Compound

VOC structure

Earthy

Actinomadura sp., Micromonospora sp., Nocardioides sp., Streptomyces sp.

Geosmin

Open image in new window

Musty

Micromonospora sp., Nocardioides sp.

2-Methyl-isoborneol

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Earthy, musty

Streptomyces sp.

Geosmin, 2-methyl-isoborneol

 

Moldy, musty

Actinobacteria

2-Isopropyl 3-methoxypyrazine

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Woody, earthy

Actinobacteria including Streptomyces sp.

Cadin-4-ene-1-ol

Open image in new window

Moldy, musty

Actinobacteria including Streptomyces sp.

2,4,6-Trichloroanisole

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Moldy, musty

Actinobacteria

Chloroanisole

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8.3.1 Geosmin

Geosmin is an organic compound, first identified in Actinobacteria by Gerber and Lechevalier (1965), with a molecular formula of C12H22O and a molecular weight of 182.3 g/mol. The term “geosmin” means “earth odor.” The molecular structure of this compound shows a bicyclic tertiary alcohol. It is produced both intracellularly and extracellularly, and it is released into the water when these microbes die. In acidic conditions, geosmin decomposes into odorless substances such as argosmin; hence, vinegar and other acidic ingredients are used in fish recipes to reduce the muddy flavor. This earthy-smelling compound is also observed in cured meat, dried beans, canned mushrooms, and other root crops (Lloyd and Grimm 1999; Maga 1987). This compound is also responsible for an earthy taste and odor problems in drinking water supplies (Table 8.2). The odor threshold concentration for geosmin is 1–10 ng/L at 45 °C (McGuire et al. 1981; Rashash et al. 1997).

8.3.2 2-Methyl-Isoborneol

2-Methyl-isoborneol is a bridged aliphatic structure, which was first found as a natural metabolite of Actinobacteria and named “methylisoborneol” by Gerber (1969). In addition, Rosen et al. (1970) determined that 2-methyl-isoborneol was produced by Actinobacteria in natural waters. It was subsequently shown to be produced as a secondary metabolite by different species of Cyanobacteria and Actinobacteria. 2-Methyl-isoborneol is characterized by an earthy–musty odor, which can be detected by people at very low concentrations (Table 8.2). The odor threshold concentration of 2-methyl-isoborneol is 5–10 ng/L, and its molecular formula and molecular weight are C11H20O and 168.28 g/mol, respectively.
Table 8.2

General characteristics of geosmin and 2-methyl-isoborneol: physical and chemical properties and odor threshold (Juttner and Watson 2007)

Characteristic

Geosmin

2-Methyl-isoborneol

Molecular formula

C12H22O

C11H20O

Molar mass (g/mol)

182.3025

168.2759

Boiling point at 101.325 kPa (°C)

270–271

207–209

Flash point (°C)

103.89

83.33

Vapor pressure (Pa)

5.56

6.76

Odor threshold (μg/L)

0.015

0.35

Structure

Open image in new window

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8.3.3 Chemical Compounds Behind the Smell of Rain

After the first rain, we smell a very exclusive and pleasant earth odor. This earthy odor is known as geosmin. The Gram-positive Eubacterium, Actinobacteria and, in particular, Streptomyces which also represent the normal flora in soil and waterare the causative agents of geosmin odor. Actinobacteria, including Streptomyces are adapted to dry, desiccated, or moist climate conditions. During rain, they readily form spores which are stress resistant and can survive under desiccation or extreme heat. Geosmin is chemically dimethyl-9-decalol. It is contained in the spore coat of soil bacteria. When raindrops strike the ground, soil containing spores is spread into the air. The spores are microscopic, circular, and more lightweight than the soil particles. They remain suspended as a soil–water aerosol, and when we inhale the aerosol, we smell the geosmin present in the spores. Because these bacteria generally do not form spores in moist soil, which is formed after first the rain, they relapse back to their filamentous vegetative form. They are present as spores in the soil only before the start of rain, when the weather is already dry or is warm and damp, so there are no spores present in wet conditions and therefore no geosmin odor present in the environment.

The most important thing is that these bacteria are found in all types of soils, and in fresh and aquatic water sources, all over the world. Therefore, every Homo sapiens smells enormous amounts of these odor compounds (Fig. 8.1). Chater et al. (2002) have sequenced the genome (of 8000 genes) of the S. coelicolor A3 strain, which produces many chemicals, including geosmin. Simons (2003) has suggested that camels can detect the smell of geosmin released by Streptomyces miles away on wet ground, and can track the geosmin to find an oasis; in return, the camels carry away and disperse the spores of Streptomyces .
Fig. 8.1

Detection of geosmin odor by mammals: (a) Streptomyces culture; (b) spore germination; (c) aerial mycelium formation; (d) chemical structure of geosmin; (e) mammalian inhalation of geosmin

8.4 Odor-Producing Streptomyces in Different Habitats

Geosmin and 2-methyl-isoborneol are produced by members of Streptomyces found in soil and water sources such as lakes, reservoirs, and running water. In addition, there are several other biological sources that are often overlooked, notably those that originate from terrestrial ecosystems (Table 8.3).
Table 8.3

Streptomyces species that produce geosmin and 2-methyl-isoborneol

Streptomyces strains

Compounds

Reference

S. odorifer

2-Methyl-isoborneol

Gaines and Collins (1963)

S. antibioticus IMRU 3720

Geosmin

Gerber and Lechevalier (1965)

S. fradiae IMRU 3535

Geosmin

Gerber and Lechevalier (1965)

S. griseus LP-16

Geosmin

Gerber and Lechevalier (1965)

S. alboniger 12464

Geosmin

Gerber (1967)

S. lavendulae 3440 1-Y

Geosmin

Gerber (1967)

S. viridochromogenes 94

Geosmin

Gerber (1967)

S. griseoluteus IMRU 3718

Geosmin

Rosen et al. (1968)

S. antibioticus Nr. 5234

2-Methyl-isoborneol

Medsker et al. (1969)

S. griseus ATCC 10137

2-Methyl-isoborneol

Medsker et al. (1969)

S. odorifer ATCC 6246

2-Methyl-isoborneol

Piet et al. (1972)

S. odorifer ATCC 6246

Geosmin

Piet et al. (1972)

S. albasporeus, S. filipinensis, S. resistomycificus

Geosmin, 2-methyl-isoborneol

Kikuchi et al. (1973)

S. paraecox ATCC 3374

2-Methyl-isoborneol

Medsker et al. (1968)

S. lavendulae CBS 16245

2-Methyl-isoborneol

Gerber (1979)

S. tendae

Geosmin

Dionigi et al. (1992)

S. halstedii

2-Methyl-isoborneol, geosmin

Schrader and Blevins (2001)

Streptomyces sp.

2-Methyl-isoborneol, geosmin

Klausen et al. (2005)

S. malaysiensis

2-Methyl-isoborneol, geosmin

Tung et al. (2006)

Streptomyces sp.

Geosmin, 2-methyl-isoborneol

Zuo et al. (2009)

Streptomyces sp.

Geosmin

Schrader and Summerfelt (2010)

Streptomyces sp.

Geosmin, 2-methyl-isoborneol

Petersen et al. (2014)

8.4.1 Odor-Producing Streptomyces in Freshwater

The presence of substances that impart disagreeable taste and odor to drinking water is one of the principal causes of complaints from consumers. These substances may be present because of artificial or natural processes, and often result from microbial growth and metabolism. Surface waters—including reservoirs, natural lakes and rivers, and water tanks—are important sources of drinkable water throughout the world but often contain sporadic matter with an earthy–musty odor and flavor.

The major causes of odor problems associated with drinking water supplies are biological activity in water sources, especially that of Actinobacteria (Streptomyces, Nocardia, and Microbispora species) and Cyanobacteria (Oscillatoria, Anabaena, and Aphanizomenon species) (Juttner and Watson 2007). Zaitlin et al. (2003) investigated the role of Actinobacteria in the production of odorous compounds from the Elbow River—an important drinking water source for the city of Calgary in Ontario, Canada—and the results showed that the Elbow River had a high concentration of Actinobacteria, with a mean count of 256 colony-forming units (CFU) per milliliter. Actinobacteria, including Streptomyces have also been found of soft deposits in drinking water distribution pipes, at counts of 1.5 × 103 CFU L−1 (Zacheus et al. 2001).

However, it is still debatable as to whether Actinobacteria are capable of active growth in open water; the evidence suggests that they are active on submerged substrates. Isolates of Streptomyces capable of high levels of geosmin production have been found in association with zebra mussels, although it was not determined whether this bacterium was associated with a specific tissue or fecal/biofilm material (Zaitlin et al. 2003). Actinobacteria, including Streptomyces produce geosmin and 2-methyl-isoborneol, which lower the quality of surface water used for drinking. Combined microautoradiography and catalyzed reporter deposition–fluorescence in situ hybridization (CARD-FISH) analysis have been used to study the distinctiveness and activity of Actinobacteria in a freshwater environment, and 1.3 × 108 Actinobacteria per liter were found in a reservoir (Nielsen et al. 2006).

8.4.2 Odor-Producing Streptomyces in Aquaculture

Muddy–earthy–musty odors are generally known to be associated with wild-caught freshwater fish (Tucker 2000; Howgate 2004), although the occurrence of such odors has also been reported for a diverse range of freshwater aquaculture species (Lovell 1983; Yamprayoon and Noomhorm 2000; Robertson et al. 2005; Petersen et al. 2011). The source of muddy–earthy–musty flavors in freshwater fish is commonly acknowledged as originating from two compounds: geosmin and 2-methyl-isoborneol. Geosmin and 2-methyl-isoborneol are metabolites of certain groups of algae, Actinobacteria, and Cyanobacteria (Tucker 2000), and are found in various water sources such as lakes, reservoirs, and running water (Juttner and Watson 2007).

Wohl and McArthur (1998) studied samples of aquatic vegetation from three stream sites located within the Savannah River site in South Carolina, USA, and identified 32 distinct Actinobacteria strains. More than 45% of the Actinobacteria colonies isolated were Streptomyces. Of the 32 distinct strains identified, 34% were strains of Streptomyces, while Pseudonocardia, Nocardia, Micromonospora, and Actinoplanes each accounted for an additional 10% of the diversity, so a high level of Streptomyces occurred in the river and produced the musty odor. Klausen et al. (2005) found that the existence of the odorous geosmin and 2-methyl-isoborneol in freshwater environments indicated that odor-producing Actinobacteria were present in one oligotrophic and two eutrophic freshwater streams, as well as in aquaculture connected to those streams, in Denmark. Sequencing of 16S ribosomal RNA (rRNA) genes in eight bacterial isolates with typical Actinobacteria morphology from those streams and ponds demonstrated that most of them belonged to the genus Streptomyces.

The lowest geosmin concentrations were measured in the oligotrophic Funder Stream (1.0–2.4 ng L−1), while higher concentrations occurred in the eutrophic Holtum and Vorgod Streams (2–6 ng L−1, except for one finding of 12 ng L−1 in June 2003). 2-Methyl-isoborneol concentrations of 2 ng L−1 in the Vorgod Stream (in December 2002) and 9.6 ng L−1 in the Holtum Stream were measured.

Schrader et al. (2005) isolated geosmin and 2-methyl-isoborneol in recirculating aquaculture systems. Certain species of Cyanobacteria are responsible for these problems in pond-cultured fish. In these ponds, Actinobacteria, including Streptomyces, were isolated from the settling unit of recirculating aquaculture system (RAS) 1 and the standpipes of RAS 1 and RAS 5. Geosmin levels were significantly higher in biosolid samples (mean values from six RASs: 9200 ng/kg and 36,400 ng/kg in the settling unit and the standpipe, respectively) than in water samples from the settler inflow and outflow (2.3 ng/L and 2.8 ng/L, respectively) and the side-drain inflow and outflow (2.8 ng/L and 3.2 ng/L, respectively).

8.4.3 Odor-Producing Streptomyces in Soil

Soil is a complex, nutrient-poor, and highly heterogeneous environment consisting of both water- and air-filled pores (Young et al. 2008). Due to the physical properties, such as low molecular weight, lipophilicity, high vapor pressure, and low boiling points, soil contains a number of soildwelling bacteria (Actinobacteria), which produce compounds such as geosmin. They secrete it into the surrounding soil, and it is then disturbed by rainfall, spreading through the air. Geosmin is associated with Streptomyces spores, which are present in huge numbers in many soils. We can safely assume that a time traveler from today who visited the planet as it was about 440 million years ago would find the smell of the soil familiar, as the earliest land plants collaborated with the first Streptomyces to generate protocompost.

VOCs released from soil can be derived from abiotic processes (Warneke et al. 1999), but most of the compounds that are emitted are likely to be products of root or microbial (i.e., bacterial and fungal) metabolism (Bunge et al. 2008; Mayrhofer et al. 2006). Some of the most common types of VOCs emitted from soils and litters include monoterpenes, alcohols, and ethers (Stotzky and Schenck 1976; Leff and Fierer 2008), but the types and quantities of VOCs released during microbial decomposition are highly variable and influenced by the nature of the substrate. Such differences could be driven by changes in various soil characteristics, including the microbial community composition, microbial biomass, carbon substrate characteristics, redox status, nutrient availability, and moisture status. VOCs may also act as a carbon source for microorganisms, increasing soil carbon dioxide production and decreasing nitrogen mineralization rates (Paavolainen et al. 1998; Mackie and Wheatley 1999; Amaral and Knowles 1997).

Zuo et al. (2009) studied Actinobacteria, which are major producers of the typical odorous compounds geosmin and 2-methyl-isoborneol in terrestrial soil environments. Most Actinobacteria can produce spores, which can survive under extreme conditions and are dispersed extensively by wind and water flow (Goodfellow and Williams 1983). Many reports have shown that episodes of high terrestrial runoff may introduce Actinobacteria and their secondary metabolites (geosmin and 2-methyl-isoborneol) into surface waters, resulting in odors (Zaitlin et al. 2003). Recently, Forbes and Perrault (2014) isolated volatile compounds from soil and air samples; a total of 249 VOCs of interest were detected, many of which were present in soil samples (60%) and in air samples (17%).

8.4.4 Odor-Producing Streptomyces in Sediment

Sediments are an important reservoir of nutrients that are potentially available for Streptomyces fabrication, with their abundance often being correlated with sediment nutrient status. Sediments and muds in freshwater environments have, for some time, been recognized as a possible habitat for Actinobacteria growth and odor and flavor production (Adams 1929; Thaysen 1936; Issatchenko and Egorova 1944; Bays et al. 1970). Furthermore, sterilized sediment has been found to produce geosmin (460 ng kg−1) after inoculation with S. albidoflavus.

In addition to those sources of geosmin and 2-methyl-isoborneol, Actinobacteria have also been found to produce musty odors in sediments (Schrader and Blevins 1993). However, systematic investigations into the abundance and taxonomy of the Actinobacteria that are responsible for geosmin and 2-methyl-isoborneol production in sediments are still lacking. Sugiura and Nakano (2000) studied 40 isolates of Actinobacteria species from the sediment of Lake Kasumigaura in Japan, which has a mean depth of 4.0 m, and found that they produced both geosmin (approximately 60 mg kg−1 of dry weight (dw)) and 2-methyl-isoborneol (approximately 50 mg kg−1 dw) in cultures grown in BS medium. In 2006, Tung et al. studied odor-producing Streptomyces isolated from the mud of the Feng-Shen reservoir, and the results showed that S. malaysiensis (identified by using M liquid cultures) produced geosmin concentrations of up to 4.5 ng mg−1 and 2-methyl-isoborneol concentrations of up to 2.4 ng mg−1. Similarly, Zuo et al. (2010) reported high levels of geosmin occurring in the sediments of the Xionghe reservoir, which has a mean depth of 13.2 m. Up to 5280.1 ng kg−1 dw of geosmin was detected in the sediment, and eight strains of Streptomyces isolated from the sediment were confirmed as producers of geosmin and 2-methyl-isoborneol, detected by headspace solid-phase microextraction–gas chromatography–mass spectrometry (HSPME-GC-MS) analysis. On the basis of in situ analysis and the production of odorous compounds by the isolated Actinobacteria, it was concluded that the geosmin in sediments was produced by species of Streptomyces. The concentrations of geosmin in the overlying water were significantly correlated with those in the sediments (r = 0.838, p < 0.05). The geosmin in the overlying water was released from the sediments and, consistent with the findings of in vitro studies, the percentage release was between 21.4% and 51.4% over 12 d.

8.5 Biosynthesis of Geosmin

Bentley and Meganathan (1981) were the first researchers to investigate the biosynthetic pathway of geosmin and 2-methyl-isoborneol metabolism, using radio-gas chromatography. The original results reported by Bentley and Meganathan favored the mevalonate pathway for Streptomyces on the basis of the production of labeled geosmin and 2-methyl-isoborneol from labeled acetate. These researchers proposed that geosmin and 2-methyl-isoborneol were synthesized through an isoprenoid pathway (also known as the terpenoid or mevalonate pathway), with 2-methyl-isoborneol having a monoterpene precursor (geranyl pyrophosphate) and geosmin a sesquiterpene precursor (farnesyl pyrophosphate). Figure 8.2 shows a simplified biosynthetic pathway for the formation of 2-methyl-isoborneol and geosmin in Streptomyces and myxobacteria (Friedrich and Watson 2007).
Fig. 8.2

Biosynthetic scheme for the formation of 2-methyl-isoborneol and geosmin in Streptomyces and myxobacteria

The latter pathway may function exclusively in the synthesis of geosmin and other isoprenoids in some groups such as myxobacteria and may contribute to geosmin production in the stationary growth phase of Streptomyces . Several studies have also confirmed the same pathway for Streptomyces and Cyanobacteria. Dionigi et al. (1992) studied the effects on the growth and metabolism of the geosmin-producing Actinobacteria S. tendae and revealed that farnesol can inhibit the geosmin synthesis process, in turn suppressing geosmin-producing species.

The terpenes produced in Streptomyces species give the impression of being derived from either the mevalonate-dependent or mevalonate-independent pathways. Cane and Watt (2003) and Gust et al. (2003) identified a germacradienol synthase enzyme (Cyc 2 protein) from S. coelicolor that is needed for the biosynthesis of geosmin. Singh et al. (2009) experimentally proved that important production of an intracellular pool of acetyl coenzyme A (acetyl-CoA) after deletion of the doxorubicin biosynthetic pathway led to improved growth and longer survival of the cell culture. Likewise, greater accumulation of acetyl-CoA led to biosynthesis of geosmin in S. peucetius. As the concentration of geosmin synthase increased, production of geosmin increased in tandem in the presence of adequate acetyl-CoA and the rate of enzyme activity rose in direct proportion to the increase in the substrate concentration.

However, a more recent study with S. coelicolor revealed that germacradienol synthase is a multifunctional enzyme with the N- and C-terminal domains each harboring a distinct functional active site (Jiang et al. 2007). The N-terminal is responsible for catalyzing the cyclization of farnesyl diphosphate (FPP) to germacradienol, and C-terminal catalyzes the conversion of germacradienol to geosmin. Likewise, Komatsu et al. (2008) found that of six Streptomyces species that were tested, S. ambofaciens, S. coelicolor A3, S. griseus, and S. lasaliensis produced 2-methyl-isoborneol. The regions containing monoterpene cyclase and methyltransferase genes were amplified by using PCR from S. ambofaciens and S. lasaliensis, respectively, and their genes were heterologously expressed in S. avermitilis, which was naturally deficient in 2-methyl-isoborneol biosynthesis by insertion and deletion; all exoconjugants of S. avermitilis produced 2-methyl-isoborneol.

8.5.1 Environmental Conditions That Favor Geosmin Production

Being a secondary metabolite, geosmin is produced by Streptomyces during secondary mycelial growth coinciding with sporulation. This has been demonstrated by the inhibition of geosmin production by Streptomyces mutant strains that are incapable of aerial mycelium development, as well as by normal growth on media not conductive to sporulation (Bentley and Meganathan 1981; Dionigi et al. 1992). In the presence of aerial mycelium and spores to correspond with the excretion of terpenoid compounds, whereas nondifferentiating strains either did not excrete such compounds or released them only to a limited extent. The aerial mycelium, which ultimately produces spores, develops from the substrate mycelium accompanied by lysis of the substrate hyphae. During this transition phase, Streptomyces species are particularly susceptible to competition from other organisms, and many secondary metabolites (i.e., antibiotics) appear in this growth phase, with the production of geosmin and 2-methyl-isoborneol by Streptomyces cultures exhibiting more morphological differentiation (Scholler et al. 2002; Tung et al. 2006).

As the secondary mycelial stage of growth is obligatorily aerobic, Streptomyces require the presence of oxygen for geosmin and 2-methyl-isoborneol production. Schrader and Blevins (1999) reported that increased geosmin production occurred in Streptomyces cultures in the presence of higher concentrations of atmospheric oxygen. Sunesson et al. (1997) observed that the carbon dioxide concentration also affected geosmin production by S. albidoflavus, with an elevated concentration (10% carbon dioxide atmosphere) being observed to decrease geosmin production. However, Schrader and Blevins (1999) observed more geosmin production in cultures of S. halstedii grown in a 10% carbon dioxide atmosphere than in those grown in 5% or ambient carbon dioxide concentrations. Despite being neutrophiles, these bacteria have been detected in both moderately acidic (pH 5) and alkaline (pH 9) aquatic environments (Jiang and Xu 1996).

Blevins et al. (1995) showed that S. halsetdii grew optimally in a neutral pH range (6–7) but, interestingly, the highest geosmin production occurred at pH 9 and in the extensive range of pH 6 to 11. Similar observations were reported by Yagi et al. (1987). Certainly, temperature is an important parameter affecting the metabolic activity of Streptomyces , which are predominately mesophilic and exhibit optimum growth between 25 °C and 30 °C (Goodfellow and Williams 1983). Likewise, Wood et al. (1985) determined that the minimum temperature for geosmin production by S. albidoflavus in nutrient-amended reservoir water was 15 °C and that all documented cases of earthy odor problems occurred when the water temperature exceeded this. Recently, Zuo et al. (2010) established that some sediment isolates of Streptomyces could grow slowly and produce relatively low concentrations of geosmin at 4 °C and 10 °C.

8.5.2 Purpose of Geosmin Biosynthesis

The production of geosmin and 2-methyl-isoborneol coincides with Streptomyces morphological differentiation and sporulation, suggesting that the possible biological purpose of these metabolites is related to the reproductive phase of the life cycle of these bacteria (Bentley and Meganathan 1981; Dionigi et al. 1992). Similarly, Scholler et al. (2002) and Tung et al. (2006) reported that volatile metabolite compounds isolated from actinobacterial species played a main role in biological function. However, many other secondary metabolites, they may serve as a defense strategy, to antagonize rival microorganisms in times of harsh conditions (e.g., nutrient limitation) when their reproductive growth is initiated to ensure the survivability of the next generation of germinating spores. The low-level toxicity of geosmin and 2-methyl-isoborneol to higher-order organisms is evident from numerous studies (Nakajima et al. 1996; Burgos et al. 2014).

Zaitlin and Watson (2006) maintain that the high concentrations used in these studies, which greatly exceeded those typically encountered in freshwater environments, may be encountered by organisms near sources of microorganisms or at the microscale level in sediments, soil, and biofilms. Similarly, Watson (2003) reported that the water industry has tended to treat geosmin and 2-methyl-isoborneol as metabolic waste products, but it seems unlikely that they would play no adaptive biological role, given the complexity and energetic costs of their biosynthesis and the ubiquity of these compounds in nature. Terpenoids have a possible biological function as antimicrobial compounds, as well as playing alternative adaptive roles in the life of Streptomyces . More recently, these and many other secondary metabolites have been re-examined for their potential bioactivity, to understand the triggers, mode, and dynamics of their production (Watson 2003; Watson and Cruz-Rivera 2003).

8.6 Geosmin Detection

Previous analytical methodologies for the analysis of geosmin and 2-methyl-isoborneol have included closed-loop stripping and conventional purge-and-trap techniques. Closed-loop stripping involves large sample volumes and an adsorbent bed, which must be eluted properly for accurate compound quantization. With a purge-and-trap technique, large enough sample volumes cannot be easily analyzed to obtain the sensitivity required without encountering technological challenges. One current and effective way to measure the concentrations of taste and odor compounds in raw and finished water sources is solid-phase microextraction (SPME) followed by GC-MS detection (Fig. 8.3). The SPME method utilizes a SPME fiber that is exposed to the headspace of the sample being evaluated. Target compounds from the sample are adsorbed onto the fiber coating and then thermally desorbed from the fiber in a heated injection port.
Fig. 8.3

Geosmin production and laboratory analysis of volatile organic compounds (VOCs) and water-soluble small molecules by solid-phase microextraction (SPME), closed-loop stripping analysis (CLISA), and gas chromatography–mass spectrometry (GC-MS), Headspace-gas chromatography (HS-GC), secondary electrospray ionization-mass spectrometry (SESI-MS), selected ion flow tube mass spectrometry (SIFT-MS), proton transfer reaction mass spectrometry (PTR-MS), Ion molecule reaction mass spectrometry (IMR-MS)

This method has recently been accepted and published as standard method 6040 D for analysis of taste and odor compounds. The method is sensitive to odor compounds down to low single-digit parts per trillion (ppt), reporting limits using quadrupole or ion-trap MS.

Recent technology for geosmin detection includes GC-MS, which allows highly sensitive measurement of metabolites at levels as low as parts per trillion. This method, however, can require large sample volumes and intensive sample concentration procedures such as liquid–liquid extraction, closed-loop stripping analysis (CLISA)—which requires complex equipment—simultaneous distillation extraction, or purge-and-trap techniques, all of which can result in low sample throughput due to lengthy protocols (Watson et al. 2000). The high-resolution mass spectrometers required for detection of low concentrations are extremely costly. Sensory analysis of geosmin by human assessment is a simple method for detection but relies upon the sensing capabilities of the individual and has several limitations, with the lack of quantification being paramount. Hence, sensing of geosmin is strictly qualitative and is not a suitable technique for measuring concentrations in drinking water sources. Enzyme-linked immunosorbent analysis (ELISA) uses antibodies to detect geosmin and provides a rapid field test for geosmin detection; however, it is costly and its detection threshold (1 μg L−1) is too high to be of any practical value.

8.6.1 Analytical Methods Involved in Geosmin Detection

Analytical methods are designed to separate, isolate, identify, and quantify analytes of interest within a sample. There are various techniques, and there have been various reviews on the separation of these components, specifically in mammals. With regard to characterizing odorous compounds, the most frequently implemented analytical techniques are gas chromatography (GC), gas chromatography–mass spectrometry (GC-MS), gas chromatography–flame ionization detection (GC-FID), gas chromatography–time-of-flight mass spectrometry (GC-TOF-MS), nano–liquid chromatography–mass spectrometry (nano-LC-MS), matrix-assisted laser desorption/ionization–time-of-flight mass spectrometry (MALDI-TOF-MS), electrospray ionization–mass spectrometry (ESI-MS), gel electrophoresis, thin-layer chromatography (TLC), and gas liquid chromatography (GLC).

In GC—the most widely used analytical tool—a mixture of VOCs is separated into individual VOCs and semi-VOCs, which are eluted out of the GC column at different times. This allows quantification and qualification of the compounds within the mixture. Another reason for the common implementation of GC is that it can analyze volatile compounds that can be detected via the olfactory system. Use of GC-MS to identify compounds is more efficient than use of other detectors because it has an extensive library available (the US National Institutes of Standards and Technology (NIST) electron ionization–mass spectrometry (EI-MS) database), with over 200,000 entries for comparison matching.

In our recent study, a total of 26 actinobacterial isolates were used for the screening of odor-producing compounds. Out of 26 isolates, 13 were isolated from soil samples collected at three different locations in Tiruchirappalli, Tamil Nadu, India. On the basis of morphological appearance, the actinobacterial isolates were identified as Streptomyces , Actinopolyspora, Saccharopolyspora, and Actinomadura species (Fig. 8.4). Further, the actinobacterial isolates were screened for their ability to produce odor metabolites. Among the 26 tested actinobacterial cultures, only isolate SD7 exhibited excellent odor production, with a total score of 4.0, while the Streptomyces species DDBH005 showed good odor production, with a score of 3.14. Nine other isolates revealed moderate odor production, with scores in the range of 2.0–2.86, while 15 isolates demonstrated poor odor production, with scores in the range of 1.12–1.86. On the basis of the olfactory analysis and growth profile of Streptomyces species, cultures of Streptomyces species SD2 and LD23 were selected as potent odor producers and subjected to detection of the genes responsible for odorous compound production, as well as identification of odorous metabolites. Amplification of the geoA gene was performed using the primers 245F and 551R, in which no bands were obtained for both Streptomyces species SD2 and LD23. This could be due to the nonexistence of the geoA gene in Streptomyces species SD2 and LD23 or incompatibility of the selected primers for amplification of the geoA gene. Further, the GC-MS analysis results illustrated that both isolates contained the volatile odor compound 2-methyl-isoborneol.
Fig. 8.4

Cultural morphology of odor-producing Actinobacteria isolates in starch casein agar

GC-MS analysis was performed to determine the presence of odor compounds in Streptomyces species SD2, in which the presence of hydrocarbon-derived compounds was observed, indicating the existence of individual volatile compounds in high proportions. Figure 8.5 shows the GC-MS spectrum of Streptomyces species SD2, with two main peaks with retention times of 7.498 min and 9.89 min, corresponding to 2-methyl-isoborneol and germacradienol, respectively. The molecular mass of 2-methyl-isoborneol was found to be 168.2 g/mol, whereas that of germacradienol was 223 g/mol.
Fig. 8.5

Gas chromatography–mass spectrometry (GC-MS) of odor compounds derived from Streptomyces species SD2: 2-methyl-isoborneol (retention time 7.498 min) and germacradienol (retention time 9.89 min)

8.7 Treatment of Odor-Causing Compounds

When taste and odor problems occur in drinking water, the general water treatment process cannot remove the whole amounts of the compounds, because of the extremely low odor thresholds of geosmin of (15 ng/L) and 2-methyl-isoborneol (35 ng/L). Lalezary et al. (1986) found that conventional water treatment technologies—consisting of breakpoint prechlorination, coagulation, sedimentation, and postchlorination—are not effective in reducing geosmin and 2-methyl-isoborneol in potable water to below their odor thresholds. For this reason, advanced water treatment processes are required to remove geosmin and 2-methyl-isoborneol compounds. These advanced technologies include biological treatment, AOP, chlorination, and some integrated systems (Table 8.4).
Table 8.4

Water treatment methods for odor removal. Geosmin and 2-methyl-isoborneol in water can be removed by ozonation/biofiltration, granular activated carbon/sand biofiltration, oxidation/powdered activated carbon, and rapid mix/flocculation/sedimentation methods

Treatment technology

Findings

References

Ozonation/biofiltration

By-product (nonbiodegradable) from ozonation can be used by the bacteria as a substrate; this enhances the geosmin and 2-methyl-isoborneol removal efficiency of the biofilter

Nerenberg et al. (2000)

Oxidation/powdered activated carbon

70% geosmin and 2-methyl-isoborneol removal efficiency

Jung et al. (2004)

Granular activated carbon/sand biofiltration

86% geosmin and 52% 2-methyl-isoborneol removal efficiency

Elhadi et al. (2004, 2006)

Rapid mix/flocculation/sedimentation

70–90% geosmin and 2-methyl-isoborneol removal efficiency

Huck et al. (1995)

O3/granular activated carbon

89% removal efficiency with single O3 and >95% removal efficiency with combined O3/granular activated carbon

Young et al. (1996)

8.7.1 Biofiltration

Biofiltration is one of the methods most commonly used to remove geosmin and 2-methyl-isoborneol from drinking water. The main biofiltration systems used for geosmin and 2-methyl-isoborneol removal are activated carbon, slow sand filtration, and ultra/nanofiltration. The rates of removal of geosmin and 2-methyl-isoborneol by biofiltration are dependent on the biofilter media, biomass, temperature, and contact time. Some soil and aquatic bacteria are capable of biodegrading 2-methyl-isoborneol and geosmin, though there is no evidence of significant removal. The temperature of the water, which is typically between 10 °C and 20 °C, does not have a significant impact on removal of geosmin and 2-methyl-isoborneol.

8.7.2 Activated Carbon

Activated carbon is one of the methods most widely used to remove geosmin and 2-methyl-isoborneol in water utilities. Activated carbon can be categorized into two different systems depending upon its particle size: granular activated carbon and powdered activated carbon. In granular activated carbon, the activated carbon is used as a granular medium above the sand/gravel media filter for the removal of geosmin and 2-methyl-isoborneol from the water passing through it. Powdered activated carbon is basically used in the rapid mix stage, reacts with contaminants in the water, and is finally removed as sludge after the filtration process. Both granular activated carbon and powdered activated carbon are commonly used and are known to be effective for control of geosmin and 2-methyl-isoborneol. Although the removal of geosmin and 2-methyl-isoborneol by activated carbon reduces their levels to below their odor threshold concentrations, the complex procedure and high cost of activated carbon make the method challenging to implement in conventional drinking water treatment plants.

8.7.3 Advanced Oxidation Processing

AOP using ozone and other oxidants, combined with ultraviolet/vacuum ultraviolet, has been shown to be effective in the removal of geosmin and 2-methyl-isoborneol. Most such processes use ozone as the main oxidant to remove geosmin and 2-methyl-isoborneol. However, the oxidation reaction is known to produce disinfection by-products, which can cause birth defects and cancer. Currently, the use of ozone combined with other technologies, commonly ultraviolet radiation, is known to be effective. Lundgren et al. (1988) removed more than 95% of geosmin and 2-methyl-isoborneol by using 7 mg/L of ozone in water with 50 ng/L of 2-methyl-isoborneol and geosmin. Koch et al. (1992) used ozone dosages of 1, 2, and 4 mg/L with hydrogen peroxide (0.2 mg/mg) and improved 2-methyl-isoborneol removal by 20%.

Altogether, it is concluded that the soil Actinobacteria Streptomyces species have the ability to produce odorous compounds. Though odor production can be determined by olfactory analysis, quantitative measurements can be obtained only by dynamic instrumentation. Identification of the gene(s) responsible for production of these odor compounds requires detailed study with different gene-specific primers.

8.8 Conclusions

Geosmin and 2-methyl-isoborneol have been identified as the main taste- and odor-causing compounds in drinking water sources such as rivers, lakes, and water dams. Although these two compounds have not been associated with any serious health effects, the taste and odor resulting from their presence in the water supply are considered unsafe by consumers. Evidence for the widespread distribution, abundance, and activity of Streptomyces and other Actinobacteria in natural and man-made aquatic environments has been appraised. Cultivars of these bacteria isolated from soil, freshwater habitats including sediment, vegetation, the water mass, or more specialized substrates readily demonstrate geosmin-producing abilities and 2-methyl-isoborneol–producing abilities in vitro, and they may indeed be potent sources of earthy–musty odors. To elucidate the contribution of these bacteria to this aesthetic water quality problem, more research is required to verify their abundance and capability to be metabolically active in such habitats. Some conventional technologies are used to treat or remove geosmin and 2-methyl-isoborneol in water sources. Coagulation, sedimentation, chlorination, and ozonation have been found to be effective for their treatment. Globally, odor- and flavor-producing microorganisms significantly reduce drinking water quality in many cities, and there is a great need for alternative management practices to reduce taste and odor compounds. The first step in the development of new water treatment procedures will be to identify the dominant odor producers.

Notes

Acknowledgements

D.D. thanks the University Grants Commission (UGC), New Delhi, India, for financial support under the Raman Fellowship for Postdoctoral Research in the USA (F. no. 5-29/2016(IC) Dt.10.02.2016) and the Department of Science & Technology–Fund for Improvement of Science & Technology Infrastructure (DST-FIST) Programme (ref. no. SR/FIST/LS1-013/2012) dated August 13, 2012. S.L. is indebted to the Department of Science and Technology–Innovation in Science Pursuit for Inspired Research (DST-INSPIRE), New Delhi, India, for financial support in the form of a Junior and Senior Research Fellowship (DST Award Letter no. IF110317/DST/INSPIRE Fellowship/2011/Dt.29.06.2011).

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Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Dharumadurai Dhanasekaran
    • 1
    • 2
  • Saravanan Chandraleka
    • 3
  • Govindhan Sivaranjani
    • 1
  • Selvanathan Latha
    • 1
  1. 1.Department of Microbiology, School of Life SciencesBharathidasan UniversityTiruchirappalliIndia
  2. 2.Department of Molecular, Cellular and Biomedical SciencesUniversity of New HampshireDurhamUSA
  3. 3.Department of ChemistryUrumu Dhanalakshmi CollegeTiruchirappalliIndia

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