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Microbial Pigments Learning From Himalayan Perspec
Microbial Pigments Learning From Himalayan Perspec
https://doi.org/10.1093/jimb/kuac017
Advance access publication date: 6 August 2022
Natural Products – Review
Abstract: Pigments are an essential part of life on earth, ranging from microbes to plants and humans. The physiological and envi-
ronmental cues induce microbes to produce a broad spectrum of pigments, giving them adaptation and survival advantages. Microbial
pigments are of great interest due to their natural origin, diverse biological activities, and wide applications in the foods, Pharma-
ceuticals, cosmetics, and textile industries. Despite noticeable research on pigment-producing microbes, commercial successes are
scarce, primarily from higher, remote, and inaccessible Himalayan niches. Therefore, substantial bioprospection integrated with ad-
vanced biotechnological strategies is required to commercialize microbial pigments successfully. The current review elaborates on
pigment-producing microbes from a Himalayan perspective, offering tremendous opportunities for industrial applications. Addition-
ally, it illustrates the ecological significance of microbial pigments and emphasizes the current status and prospects of microbial
pigment production above the test tube scale.
Violacein, deoxyviolacein Iodobacter sp. PCH194 Bhoot ground kettle lake, Antimicrobial, anticancer, and Kumar et al., (2021)
(violet color) Sach Pass, Himalaya, UV protecting properties
India
Red pigment Rhodonellum psychrophilium Pangong Tso Lake located in Antibacterial, antioxidant, Bisht et al., (2020)
Leh Ladakh, India growth stimulating
properties
Yellow color Flavobacterium spp. Laigu, Zepu, Renlongba, and Adaptation under Liu et al., (2019)
Gawalong glaciers, low-temperature conditions
Tibetan Plateau
Various pigments (pink, - Tirich Mir glacier, Hindu - Rafiq et al., (2019)
yellow, and orange) kush Himalaya
Yellow, orange, brown, Proteobacteria, Firmicutes, Himalayan glaciers, Adaptation against cold Panwar et al., (2019)
violet, and pinkish-red Actinobacteria, Uttarakhand, India temperature
Bacteroidetes
Carotenoid (orange) Penicillium sp. Indian Himalayan region Antimicrobial potential Pandey et al., (2018)
Carotenoids (various colors) Proteobacteria, Yuzhufeng glacier, Tibetan - Shen et al., (2018)
Actinobacteria, Plateau
Bacteroidetes, and
Firmicutes
Prodgiosin (red pigment) Serratia nematodiphila RL2 Lahul and Spiti, Himalaya, Antibacterial activity Gondil et al., (2017)
India
Carotenoids (yellow-orange) Sanguibacter suarezii KK6, Leh and Ladakh, India Survival strategies in cold Kushwaha et al.,
Kocuria turfanensis KK7, conditions (2014)
Kocuria rosea KK12,
Planococcus maritimus
KK21
Various pigments Firmicutes, alpha- and East Rongbuk glacier, Mount Adaptation against stress Shen et al., (2012)
gamma-Proteobacteria, Everest
Actinobacteria
Yellow pigment Leifsonia pindariensis Pindari glacier, Indian - Reddy et al., (2008)
Himalayas
Yellow, pink, orange Bacillus odyssey, Puruogangri glacier, Tibetan - Zhang et al., (2008)
Flavobacterium sp. Plateau
Cryobacterium
psychrophilum, Kocuria
carniphila, Frigoribacterium
sp.
Violacein (violet) Janthinobacterium lividum Xinjiang glacier, China Survival strategies in cold Lu et al., (2009)
XT1 conditions
reddish-orange (24%), orange (16%), white (11%), pink (2%), and The pigment identified as prodigiosin showed an antibacterial
brown (<1%) were obtained from the ice core (Shen et al., 2018). effect against various pathogenic bacteria. Another red pigment-
HPLC analysis showed that 40% of the pigments were α-carotene, producing bacterium Rhodonellum psychrophilium GL8 was isolated
followed by 28% diatoxanthin. Other pigments identified were from a high-altitude lake, Pangong Tso, Leh, India (Bisht et al.,
β-carotene, fucoxanthin, peridinin, and zea/lutein. Pigmented 2020). The pigments were a mixture of prodigiosin and other
bacteria were also isolated from soil, water, and ice samples from related compounds and showed antimicrobial, antioxidant, and
the western Himalayas in Uttrakhand, India, with varying alti- bioenhancer properties. Blue-violet color-producing bacteria were
tudes from 2300 to 4500 masl (Panwar et al., 2019). Amongst, also discovered in the high-altitude Himalayas. For example, the
some of the bacterial pigments showed intense antioxidant ac- violacein-producing psychrotrophic bacterium Janthinobacterium
tivity. These extensive diversity studies showed the abundance of lividum XT1 was isolated from a glacier in Xinjiang, China (Lu
pigment-producing bacteria in the high-altitude glaciers. et al., 2009). A unique eurypsychrophilic bacterium, Iodobacter sp.
PCH194, capable of violacein pigment production, was isolated
from the sediments of Bhootground kettle lake situated at 4200
Characterization of Pigments from the masl in Sach Pass, western Himalaya, India (Kumar et al., 2021).
Bacteria/Fungi The violacein pigment was a mixture of violacein and deoxyvi-
Apart from the extensive diversity studies, only a few were olacein and had promising antimicrobial and anticancerous
reported to isolate and characterize pigments from bacteria. For properties. The yellow-colored Flavobacterium spp. were isolated
instance, a red pigment-producing Serratia nematodiphila RL2 was from Tibetian glaciers, and their genome possesses genes en-
isolated from the cold desert of Lahaul valley (Gondil et al., 2017). coding for carotenoid biosyntheses, such as phytoene synthase,
4 | Journal of Industrial Microbiology and Biotechnology, 2022, Vol. 49, No. 5
Fig. 2. Pigment producing bacteria isolated from high-altitude trans-Himalayan region: (a) Iodobacter sp. PCH194, (b) Streptomyces sp. PCH436, (c)
Streptomyces sp. PCH436, (d) Janthinobacterium sp. PCH410 (e) Kocuria sp. PCH206, (f) Pedobacter sp. PCH18 (g) Pseudomonas sp. PCH 413, (h) Arthrobacter sp.,
(i) Bacillus sp. PCH164, (j) Flavobacterium sp. PCH19, (k) Arthrobacter sp. PCH30, and (l) Leifsonia sp. PCH178.
lycopene-β-cyclase, and β-carotene hydroxylase (Liu et al., 2019). Co-Production of Biomolecules with Pigments as
Similarly, the abundance of genes/proteins involved in carotenoid Sustainable Bioprocess
biosynthesis was found in the whole-genome metagenomes of Besides the fundamental research, the pigment-producing mi-
high-altitude Himalayan lake sediments (Kumar et al., 2022). crobes from the Himalayas are goldmines for industrially relevant
Carotenoids and their derivatives produced by high-altitude bioproducts vis-à-vis microbial pigments. Since the Himalayan
Himalayan fungi Penicillium sp. GBPI_P155 possesses antibacterial regions are less explored, they could be a rich source for new
potential. It may be a defense strategy against other microorgan- and unique pigment-producing microorganisms. Thus, efforts
isms (Pandey et al., 2018). Similarly, many fungi produce pigments are required to explore its hidden treasures. Our lab focuses on
as an adaptive measure to cope with stress conditions of low tem- bioprospecting high-altitude Himalayan microbiomes for basic
perature, UV radiations, and oxidative stress (Pandey et al., 2018; and applied research (Kumar et al., 2018a, 2019, 2020, 2021, 2022;
Sajjad et al., 2020). It suggested that microbial pigments such as Thakur et al., 2018; Ambika et al., 2022). The isolation and iden-
carotenoids play an essential role in adaptation to the stress en- tification of various pigment-producing bacteria from the high-
vironment of high-altitude Himalayas. altitude Himalayan region were accomplished during the course.
Table 2. Biotechnological strategies for the up-scale production of bacterial pigments
Carotenoids Crude glycerol Rhodotorula glutinis TISTR 5159 Batch bioreactor 1.0 0.135 Saenge et al., (2011)
Corn steep liquor and sugar cane molasses Sporidiobolus pararoseus Batch bioreactor 1.5 0.0019 Borba et al., (2018)
Spent coffee ground Sporobolomyces roseus Fed-batch bioreactor 12.5 0.0126 Petrik et al., (2014)
Zeaxanthin Yeast extract, peptone, sodium chloride Flavobacterium sp. P8 strain Batch bioreactor 5.0 0.0312 Vila et al., (2020)
Flexirubin Lactose, tryptophan and KH2 PO4 Chryseobacterium artocarpi CECT8497 Batch bioreactor 50.0 0.52 Venil et al., (2015)
Agro-industrial waste Chryseobacterium artocarpi CEC8497 Batch bioreactor 5.0 and 50 0.54 and 0.20 Aruldass et al., (2016)
Violacein Glucose, peptone Iodobacter sp. PCH194 Batch bioreactor 7.5 and 10.0 1.5 and 1.25 Kumar et al., (2021)
Glucose Recombinant E. coli BL21 (DE3) Batch bioreactor 5.0 1.75 Fang et al., (2015)
Liquid pineapple waste and tryptophan Chromobacterium violaceum UTM5 Batch bioreactor 50.0 16. 2 Aruldass et al., (2015)
Tryptic soy broth Janthinobacterium strain UV13 Batch bioreactor 5.0 0.077 Alem et al., (2020)
Glycerol, meat extract, peptone Janthinobacterium lividum 1522 Batch bioreactor 2.0 1.80 Kanelli et al., (2018)
Prodigiosin Brown sugar (10%) Serratia marcescens UTM1 Batch bioreactor 5.0 8.0 Aruldass et al., (2014)
Glucose, glycerol Serratia marcescens 02 Batch bioreactor 5.0 5.83 Tao et al., (2005)
Peanut oil cake Serratia marcescens CF-53 Batch bioreactor 2.0 18.2 Naik et al., (2012)
Sucrose, peptone Serratia marcescens Batch bioreactor 7.0 0.39 Mohammed & Luti, (2020)
Amaranth Mannitol and soybean flour + GAUSE’S medium Streptomyces coelicolor MSIS Batch bioreactor 5.0 9.0 Mohanasrinivasan et al., (2013)
Kumar et al. | 5
6 | Journal of Industrial Microbiology and Biotechnology, 2022, Vol. 49, No. 5
A few prominent pigment-producing bacteria viz., Iodobacter Conclusion and Future Perspective
sp. PCH194 (CP025781), Kocuria sp. PCH206 (MH096001), Bacillus
Microbes require specific features to produce biologically active
sp. PCH164 (MF774150), Pedobacter sp. PCH18 (KY628836), Flavobac-
pigmented compounds on an industrial scale. These include fast
terium sp. PCH19 (KY628837), Arthrobacter sp. PCH30 (KY628848),
growth rates, scalability, high productivity, and preferably non-
Leifsonia sp. PCH178 (MF774164) (Kumar et al., 2018a, 2021; Thakur
pathogenic. Additionally, the strains should include the utilization
et al., 2018), Pseudomonas sp. PCH413 (MF774129), Streptomyces
of low-cost substrates, ease for scale-up and downstream process-
sp. PCH436 (ON080900), Streptomyces sp. PCH437 (ON080901),
ing, high productivity, and overall low production cost. The micro-
and Janthinobacterium sp. PCH410 (MZ396632). (Unpublished
bial pigment should be non-toxic, stable, and tolerant to pH, tem-
data) are shown in Fig. 2. Amongst, Iodobacter sp. PCH194
perature, and light. Bioprospecting pigment-producing microbes
was successfully demonstrated for the pilot-scale produc-
can obtain strains with desired features from extreme niches, in-
tion of violacein pigment and polyhydroxybutyrate as a co-
cluding the high-altitude Himalayas, and further apply genetic en-
product (Kumar et al., 2021). The patent for the Himalayan
gineering or strain improvement approaches to known potential
Iodobacter sp. PCH194 bioprocess for co-production of polyhy-
microbes. The cryospheric microbes can synthesize natural colors
droxybutyrate and violacein pigment has been filed (Kumar
as a protective shield against life-threatening ecological stresses.
et al., 2021). A few others are also being investigated in
Therefore, new possible sources for pigment-producing bacteria
our lab.
must be investigated. Exploring microbial pigments from newer
and extreme niches could provide novel and well-known pigment
molecules for diverse industrial applications.
Biotechnological Strategies for Microbial
Pigments Production
Supplementary Material
Bioprocess development is the key to the large-scale production of
microbial pigments. It includes the up-scale production of micro- Supplementary material is available online at JIMB (www.academic.
bial pigment followed by downstream processing. Several stud- oup.com/jimb).
ies have developed bioprocesses for pigment production, such
as carotenoids, flexirubin, violacein, and prodigiosin at ≥1.0 L
Funding
level (Table 2). Most studies employed wild microorganisms in
batch or fed-batch processes for pigment production. For exam- D.S. duly acknowledges Council of Scientific and Industrial Re-
ple, carotenoid production was reported from Rhodotorula gluti- search (CSIR), Government of India for financial support under
nis TISTR 5159, Sporobolomyces roseus, and Sporidiobolus pararoseus MLP201 and MLP0143 project. The manuscript represents CSIR-
using cheaper carbon sources (Saenge et al., 2011, Petrik et al., IHBT publication number 5000.
2014, Borba et al., 2018). Zeaxanthin, a type of carotenoid, was
produced by the Flavobacterium sp. P8 strain in a 5 L batch biore-
actor using yeast extract and peptone rich medium (Vila et al.,
Conflict of Interest
2020). However, the main problem associated with carotenoid pro- The authors declare no conflict of interest.
duction was the low yield. Flexirubin pigment was produced from
Chryseobacterium spp. in a batch bioreactor with a yield of 0.2 and
0.52 g/L (Venil et al., 2015; Aruldass et al., 2016). Prodigiosin pig- References
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