Assessing Forest Cover Loss Using Landsat Images and GIS: A Case Study in Colombian Protected Area

Abstract

The Corchal “El Mono Hernández” Fauna and Flora Sanctuary is a protected area located in northern Colombia and is home to the Pterocarpus officinalis forest. In this area, however, this forest cover is declining due to natural causes associated with a change in the hydrosedimentological dynamics. Multitemporal assessment was performed to quantify the forest loss. Landsat images from the years 1986, 1998, 2003, 2013, and 2018 were downloaded and a supervised classification was performed using four cover classes: “Pterocarpus officinalis,” “other vegetation,” “waterbody,” and “bare land.” The results showed that the vegetation cover of Pterocarpus officinalis forest had an initial extent of 865.26 ha in 1986; for the 1986–1998 period, the reduction was 60.30 ha; for the 1998–2003 period, it was 399.15 ha; and for the 2003–2013 period, it was 78.30 ha. Contrary to previous periods, in the 2013–2018 period, 79.65 ha of forest was recovered. In conclusion, Pterocarpus officinalis forest lost approximately 50% of its cover during the 1986–2018 period. This information is of great importance for government and management entities for decision-making in the conservation and restoration of this forest.

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Environ Monit Assess (2022) 194:654
https://doi.org/10.1007/s10661-022-10328-w
Perchlorate‑reducing bacteria fromAntarctic marine
sediments
RosaAcevedo‑Barrios · CarolinaRubiano‑Labrador· DhaniaNavarro‑Narvaez·
JohanaEscobar‑Galarza· DianaGonzález· StephanieMira· DayanaMoreno· AuraContreras·
WendyMiranda‑Castro
Received: 1 February 2022 / Accepted: 25 July 2022
© The Author(s), under exclusive licence to Springer Nature Switzerland AG 2022
in perchlorate, whereas P. lactis had the lowest
reduction. This study is significant as it is the first
finding of P. cryohalolentis and. P. lactis on the
Antarctic continent. In conclusion, these bacte-
ria isolated from marine sediments on Antarctica
offer promising resources for the bioremediation
of perchlorate contamination due to their ability to
degrade perchlorate, showing their potential use as
a biological system to reduce perchlorate in high-
salinity ecosystems.
Keywords Extremophiles· Halotolerant bacteria·
Psychrotolerant microorganism· Psychrophilic
bacteria· Perchlorate biodegradation· Toxicity
Introduction
Antarctica is the last pristine continent on Earth. How-
ever, human pressure in this region has increased with
the growth of research, tourism and transport activi-
ties. These activities have led to the establishment of
research stations and transfer systems, which repre-
sent potential sources of pollution (Marina-Montes
et al., 2020; Pereira et al., 2017; Prabagaran et al.,
2007; Xu et al., 2020). In addition to the direct and
transient transport of pollutants, the Antarctic region
experiences a variety of in situ chemical processes
that have not yet been fully characterised (Chambers
etal., 2014; Deng etal., 2020; Galbán-Malagón etal.,
2019).
Abstract Perchlorate is a contaminant that can per-
sist in groundwater and soil, and is frequently detected
in different ecosystems at concentrations relevant to
human health. This study isolated and characterised
halotolerant bacteria that can potentially perform
perchlorate reduction. Bacterial microorganisms
were isolated from marine sediments on Deception,
Horseshoe and Half Moon Islands of Antarctica.
The results of the 16S ribosomal RNA (rRNA) gene
sequence analysis indicated that the isolates were
phylogenetically related to Psychrobacter cryohalo-
lentis, Psychrobacter urativorans, Idiomarina loi-
hiensis, Psychrobacter nivimaris, Sporosarcina aqui-
marina and Pseudomonas lactis. The isolates grew
at a sodium chloride concentration of up to 30% and
a perchlorate concentration of up to 10,000 mg/L,
which showed their ability to survive in saline con-
ditions and high perchlorate concentrations. Between
21.6 and 40% of perchlorate was degraded by the
isolated bacteria. P. cryohalolentis and P. ura-
tivorans degraded 30.3% and 32.6% of perchlorate,
respectively. I. loihiensis degraded 40% of perchlo-
rate, and P. nivimaris, S. aquimarina and P. lactis
degraded 22%, 21.8% and 21.6% of perchlorate,
respectively. I. loihiensis had the highest reduction
R.Acevedo-Barrios(*)· C.Rubiano-Labrador·
D.Navarro-Narvaez· J.Escobar-Galarza· D.González·
S.Mira· D.Moreno· A.Contreras· W.Miranda-Castro
Grupo de Estudios Químicos Y Biológicos, Universidad
Tecnológica de Bolívar, 130010Cartagena, Colombia
e-mail: racevedo@utb.edu.co

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The Antarctic environment is affected by pollut-
ants such as perchlorate, which can have ecotoxi-
cological effects on the biota (Jackson et al., 2012;
Jiang et al., 2020; Riddle & Chapman, 2005; Rose
etal., 2012). Perchlorate is a toxic inorganic salt that
affects iodide binding in the thyroid gland and acts as
a potent endocrine disruptor; hence, it can negatively
influence the normal development of living beings
(Acevedo-Barrios etal.,2018, 2019b; Crawford etal.,
2017; Eck, 2015; Jiang etal.,2013).
Perchlorate originates both naturally and anthro-
pogenically (Brown & Gu, 2006; Isobe etal., 2013;
Vega etal., 2018). This compound is used in military
and firework industries for explosives and as a ferti-
liser. Their natural formation occurs during electrical
storms and atmospheric reactions related to chlorine
and ozone. Perchlorate has been detected in arid,
hypersaline and cold environments, including Antarc-
tica (Acevedo-Barrios etal., 2016, 2022; Ahn et al.,
2009; Cao et al., 2019; Jackson et al., 2010, 2012;
Kounaves et al., 2010; Parker, 2009) This contami-
nant is not efficiently reduced through physicochemi-
cal methods and the process is expensive and can
generate residues that must be subsequently treated;
thus, biological treatments are required for its deg-
radation (Acevedo-Barrios & Olivero-Verbel, 2021;
Kucharzyk etal., 2010; Kuppusamy etal., 2016; Sar-
ria etal., 2019; Urbansky, 2002; Ye etal., 2012).
Biological perchlorate reduction is based on per-
chlorate-reducing microorganisms (PCRM), which
use the enzyme chloride dismutase to reduce perchlo-
rate to chlorate (ClO3
−), and then to chlorite (ClO2
−).
Chlorite dismutase transforms ClO2
− into molecular
oxygen (O2) and chloride (Cl−) (Lv etal., 2020; Sarria
et al., 2019; Vega et al., 2018). Perchlorate-reducing
bacteria of the Alphaproteobacteria, Betaproteobac-
teria, Gammaproteobacteria and Deltaproteobacteria
subclasses have been identified in different environ-
ments, including crystal clear water and Antarctic soil
and lakes (Wang etal., 2020; Zhu etal., 2016). Ant-
arctica has a high diversity of bacterial genera of vari-
ous classes. These psychrotolerant and psychrophilic
bacteria have been used for bioremediation because of
their ability to maintain their activity under extreme
Antarctic conditions (Abd-Elnaby etal., 2016).
The environmental conditions in Antarctica
differ from those in other regions of the planet.
Although the Antarctic climate is cold, it is not uni-
form. Thus, under these environmental conditions,
extremophilic microorganisms have adaptive mech-
anisms, biochemical versatility and the ability to
tolerate and reduce perchlorate. In addition, the
natural origination of perchlorate has been reported
in Antarctica (Jiang et al., 2013; Kounaves etal.,
2010), increasing the possibility of the presence of
perchlorate-reducing bacteria in this region. There
has been interest in isolating perchlorate-reducing
bacteria from halophilic environments because of
their ability to tolerate perchlorate and potential
reduction (Acevedo-Barrios et al., 2019a; Logan
etal., 2001; Matsubara etal., 2017). In this work,
we report the isolation of perchlorate-reducing bac-
teria from marine sediment samples from Antarc-
tica. These bacteria present properties suitable for
possible biotechnological applications and consti-
tute the basis for expanding our knowledge of salt-
tolerant bacteria that can reduce perchlorate.
Materials andmethods
Study area and sample collection
Samples were obtained from marine sediments
on Deception (62°58′35″ S, 60°40′31″ W), Half
Moon (62°35′44″ S; 59°54′12″ W and 62°35′
42.4″ S; 59°55′05.1″ W) and Horseshoe Islands
(67°49′26.08″S; 67°17′22.88″W) (Fig.1) during the
III and V Colombian scientific expeditions to the
Antarctic, the “Almirante Padilla” (January–March
2017) and “Almirante Campos” (January–March
2019). Approximately 40 samples were collected in
triplicate for each experiment. A sterile spatula was
used to collect approximately 100g of sediment from
the upper 1–10 cm of the sample profile. All sam-
ples were collected in 15-mL Falcon tubes and then
refrigerated at 4°C for transport to the laboratory for
processing. Salinity and pH were recorded for each
sample, according to the methods of Nozawa-Inoue
et al. (2005). Jiang et al. (2016, 2021) previously
reported that the presence of perchlorate in Antarc-
tica is due to its natural formation in the atmosphere
to later depositing in the snow, soil and sediments.
KClO4ˉ was measured using a Thermo Scientific
Orion-93 selective perchlorate electrode (Thermo
Fisher Scientific Inc., Beverly, MA, USA) to deter-
mine the perchlorate concentration of each sample.

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Isolation and culture conditions
Isolation, purification and conservation were per-
formed as described by Acevedo-Barrios et al.
(2019a). The samples were treated with ampho-
tericin B prior to isolation. Cultivation was per-
formed in four different media with the following
compositions: Luria–Bertani (LB) medium: 10 g
of NaCl, 10g of tryptone and 5g of yeast extract;
AAD12 medium: 5g of yeast extract, 3g of sodium
citrate, 20g of MgSO4
∙
7H2O, 2g of KCl, 250g of
NaCl and 20g of agar; R2A medium: 0.5g of yeast
extract, 0.5 g of Proteose Peptone no. 3, 0.5 g of
Casamino acids, 0.5g of glucose, 0.5 g of soluble
starch, 0.3g of K2HPO4, 0.05g of MgSO4
∙
7H2O,
0.3g of sodium pyruvate and 15g of agar per litre
of laboratory quality water and M63 medium: 2.0g
of (NH4)2SO4, 13.6g of KH2PO4 and 0.0005 g of
MgSO4
∙
7H2O. These media were modified using
seawater with a KClO4
− concentration of 750mg/L.
Subsequently, the isolates were incubated at 4 °C
for 14 d under aerobic conditions. Bacterial
growth was monitored by observing the colonies.
For the conservation of the bacteria, a colony was
transferred to a cryovial with 720 μL of culture and
80 μL of glycerol and stored at −80°C, as described
by Acevedo-Barrios etal. (2019a).
Morphological characterisation
The morphology was observed using a light micro-
scope (Olympus BX41). Gram staining was con-
ducted according to Bergey’s Manual Taxonomic Key
(Boone et al., 2005) and Koneman’s Microbiologic
Atlas (Koneman etal., 2006). The isolates were incu-
bated on LB, AAD12, R2A and M63 agar.
Biochemical characterisation
Biochemical characteristics were determined using
the BBL Crystal™ Kit (Becton Dickinson Microbiol-
ogy Systems, Cockeysville, MD, USA), as described
by the manufacturer. Catalase and oxidase tests were
performed according to previously reported methods
(Boone etal., 2005).
16S rRNA gene sequencing and phylogenetic analysis
Genomic DNA of the isolated bacteria was extracted
using the DNAzol Kit (Invitrogen), according to the
manufacturer’s instructions. The 16S rRNA gene was
sequenced using the universal bacterial primers 27F (5′-
AGA GTT TGATCMTGG CTC AG-3′) and 1492R (5′-
GGT TAC CTT GTT ACG ACT T-3′) (Rubiano-Labrador
etal., 2019). Amplification of 16S rRNA was performed
Fig. 1 Geographic location
of Antarctica (a), Half
Moon Island (b), Deception
Island (c), and Horseshoe
Island (d)

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following the protocol described by Rubiano-Labrador
etal. (2019). The polymerase chain reaction (PCR) prod-
ucts were sequenced using an ABI PRISM ® 3500 system
(Laboratorio de secuenciación de ADN, Universidad
de Los Andes, Bogotá, Colombia). The resultant 16S
rRNA sequences were assembled using the sequence
editor BioEdit (version 7.2.5) (Hall,1999) and then com-
pared with data from the Ribosomal Database Project II
(RDPII). The GenBank accession numbers for the 16S
rRNA gene sequences of the isolates are MW130840,
MW130841, MZ420735, MZ420736, MZ420737,
MZ420738 and MZ420739.
Chloride susceptibility assay
All isolates were assayed for perchlorate susceptibil-
ity in LB broth in the presence of NaCl (3.5%, 5.0%,
7.5% and 30% w/v) (Bahamdain et al., 2015). The
experiments were initiated by adding 20 μL of cell
suspension (optical density (OD) = 0.6) to 5 mL of
LB broth (Acevedo-Barrios etal., 2019a).
Perchlorate susceptibility assay
All isolates were assayed for perchlorate suscepti-
bility in LB broth in the presence of perchlorate at
concentrations of 500 mg/L, 750 mg/L, 1000 mg/L,
2500mg/L, 5000mg/L, 7500mg/L and 10,000mg/L
(Fernández et al., 2005; Gholamian et al., 2011).
Experiments were performed as described for the
chloride susceptibility assay. After incubation for
14d at 4°C, the culture of each isolate was analysed
on LB agar at their corresponding KClO4ˉ concentra-
tions to confirm the viability of each bacterial isolate
(Acevedo-Barrios etal., 2019a).
Evaluation of perchlorate reduction by isolates
The experiments were performed using a KClO4ˉ con-
centration of 10000 mg/L in LB medium containing
3.5% NaCl. Inoculation of the isolates was as described
for the chloride susceptibility assay and incubation was
for 14 d at 4 °C. After incubation, the final KClO4ˉ
concentration was measured using a Thermo Scientific
Orion-93 perchlorate electrode (Thermo Fisher Scien-
tific Inc., Beverly, MA, USA), according to the man-
ufacturer’s instructions. The difference between the
concentrations before and after incubation was used to
calculate the perchlorate reduction percentage elicited
by each isolate (Acevedo-Barrios etal., 2019a).
Results
Morphological and biochemical identification
In this study, six isolations from Antarctica were used.
UTB-113 and UTB-114 were isolated from sediment
samples of Deception Island under aerobic heterotrophic
conditions at 4 °C. Both isolates were gram negative
and mobile. UTB-113 was coccobacilli shaped, whereas
UTB-114 was rod shaped. Biochemical characteristics
(for example, lactose fermentation) varied. They both pre-
sented positive catalase and negative oxidase activity and
showed positive reactions for N-acetylglucosaminidase
and nitrate reduction activity; however, they were both
negative for H2S. UTB-154 and UTB-156 were isolated
from Horseshoe Island and were gram negative, rod
shaped and both presented motility. Catalase and oxidase
reactions were positive. In addition, UTB-154 and UTB-
156 exhibited nitrate reduction and negative H2S produc-
tion. On Half Moon Island, the isolates were identified as
UTB-160, UTB-161 and UTB-162. UTB-160 was coc-
cobacilli shaped and gram negative, UTB-161 was rod
shaped and gram positive and UTB-162 was rod shaped
and gram negative. All strains isolated from Half Moon
Island presented positive catalase and oxidase reactions,
nitrate reduction and negative reactions and were negative
for H2S. The characteristics of these isolates are listed in
Table1.
Phylogenetic analysis of the isolates
The results of the phylogenetic analysis showed that
isolates UTB-113 and UTB-114 isolated from Decep-
tion Island belong to the genus Psychrobacter. UTB-
113 shares 100% sequence identity with P. cryoh-
alolentis, whereas UTB-114 shares 99.9% sequence
identity with P. urativorans. UTB-154 and UTB-156,
isolated from Horseshoe Island, belong to I. loihien-
sis and share 100% similarity. The isolates from Half
Moon Island, UTB-160 and UTB-162, share 99.9%
sequence identity with P. nivimaris and P. lactis,
respectively. Additionally, UTB-161 shares 98.8%
sequence identity with S. aquimarina.

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Table 1 Morphological and biochemical characteristics of isolates from Antarctic marine sediment samples
Characteristic UTB-113 UTB-114 UTB-154 UTB-156 UTB-160 UTB-161 UTB-162
Molecular
identification
P. cryohalolentis P. urativorans I. loihiensis I. loihiensis P. nivimaris S. aquimarina P. lactis
Source Deception Island Deception
Island
Horseshoe
Island
Horseshoe
Island
Half Moon
Island
Half Moon
Island
Half Moon
Island
Morphology Coccobacilli
shaped
Rod shaped Rod shaped Rod shaped Coccobacilli
shaped
Rod shaped Rod shaped
Colour of colony Orange White Cream Cream White Cream Light yellow
 Motility + + + + - + +
 Gram straining - - - - - + -
 Oxidase - - + + + + +
 Catalase + + + + + + +
 H2S production - - - - - - -
 Nitrate reduction + + -- + + +
 Arabinose - - - - - - -
 Galactose - - - - - - -
 Inositol - - - - - - -
 Lactose v v - - v - v
 Mannitol - - - - - - -
 Mannose - - - - - - -
 Melibiose - - - - + - -
 Rhamnose - - - - - - -
 Sorbitol - - - - - - -
 Sucrose - - - - - - -
 Adonitol - - - - - - -
 p-n-p-Phosphate - + - - - - -
 p-n-p a-ß-
Glucoside
- + - - - - -
 p-n-p-ß-
Galactoside
- - - - - - -
 Proline
nitroanilide
- - - - - - -
 p-n-p bis-
Phosphate
- - - - - - -
 p-n-p-Xyiloside - - - - - - -
 p-n-p-a-
Arabinoside
- - - - - - -
 p-n-p-
Phosphorylcholine
- - - - - - -
 p-n-p-ß-
Glucuronide
- - - - - - -
 p-n-p-N-
Acetylglucosamine
+ - - - - - -
 γ-
l
-Glutamyl
p-nitroanilide
- - - - - - -
 p-nitro-
dl
-
phenylalanine
- - - - - - -
 Urea - - - - - - -
 Glycine - - - - - - -

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Sodium chloride and perchlorate susceptibility assay
All the isolates grew in a culture medium with a
high NaCl concentration, reaching a tolerance of up
to 30% NaCl, except for UTB-161, which presented
a lower tolerance of up to 30% NaCl. In the case of
perchlorate, the concentration measured on Deception
Island ranged from 450–480mg/L; therefore, P. cryo-
halolentis and P. urativorans can tolerate this concen-
tration range of perchlorate in the environment. When
these isolates were exposed to higher concentrations
of KClO4ˉ, they grew at between 500mg/L KClO4ˉ
and 10,000 mg/L KClO4ˉ; however, they formed a
biofilm at the highest concentration. The concentra-
tion of perchlorate measured in situ on Horseshoe
Island ranged from 70 to 110mg/L, and the concen-
tration measured insitu on Half Moon Island ranged
from 180 to 220 mg/L. When I. loihiensis, P. nivi-
maris, S. aquimarina and P. lactis were exposed to
higher concentrations of KClO4ˉ, between 500 and
10,000mg/L, they grew effectively. Thus, these iso-
lates showed the ability to survive at higher concen-
trations than those recorded in their environmental
habitats.
Evaluation of perchlorate reduction by the isolates
In this study, the bacterial isolates exhibited the bio-
logical capacity to reduce KClO4ˉ (Fig.2). They were
initially exposed to 10,000mg/L and after 15d, they
reduced perchlorate between 21.6 and 40%. The bac-
teria from Deception Island, UTB-113 and UTB-114,
reduced 30.3% and 32.6% of perchlorate, respec-
tively. UTB-154 and UTB-156 isolated from Horse-
shoe Island reduced 40% of perchlorate, and bacteria
isolated from Half Moon Island, UTB-160, UTB-161
and UTB-162, reduced 22%, 21.8% and 21.6% of per-
chlorate, respectively.
+ : positive reaction, − : negative reaction, v: variable reaction.
Table 1 (continued)
Characteristic UTB-113 UTB-114 UTB-154 UTB-156 UTB-160 UTB-161 UTB-162
 Citrate - - - - - - -
 Malonic acid - - - - - - -
 Triphenyltetrazo-
lium chloride
- - - - - - -
Fig. 2 Percentage reduc-
tion of KClO4
− concentra-
tion from marine sediment
samples taken from Decep-
tion, Horseshoe and Half
Moon Islands. Effect after
15d of contact at an optical
density (OD) of 600 and
optimal pH of 7.0 ± 0.5

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Discussion
Deception Island
The isolates were taxonomically characterised based
on 16S rRNA gene sequencing and phylogenetic anal-
yses. The results showed that the three isolates belong
to the genus Psychrobacter. They were characterised
as aerobic, osmotolerant and oxidase-positive bacte-
ria and were either psychrophilic or psychrotolerant.
Psychrobacter bacteria are found in a wide range of
wet, saline and cold habitats as well as in warm and
slightly salty habitats (Bowman, 2006; Lasek etal.,
2017; Silva et al., 2018; Smith et al., 2009). Our
results are consistent with those of previous studies
on microbial communities in various Antarctic habi-
tats, where this genus was also isolated from Antarc-
tic soils (Bendia etal., 2018a; Bowman etal., 1996;
Bozal etal., 2003; Centurion etal., 2019; Che et al.,
2013; Lasek et al., 2017; Muñoz-Villagrán et al.,
2018). However, the present study represents the first
analysis of species of Psychrobacter that are associ-
ated with marine sediments from Deception Island
(Bendia etal., 2018a; Flores etal., 2018). The envi-
ronmental gradients of temperature and salinity, along
with the geochemical processes on Deception Island,
relate to the isolation of this genus. Psychrobacter has
been previously isolated from various environmental
settings owing to its diverse metabolic characteristics
(Bendia et al., 2018b; Bowman et al., 1996; Lasek
etal., 2017; Silva etal., 2018; Smith etal., 2009).
To date, Psychrobacter has been known to include
41 valid species that have been isolated from differ-
ent sources (Kokoulin etal., 2020; LPSN, n.d.). UTB-
113 and UTB-114 were identified as P. cryohalolentis
and P. urativorans, respectively. These species were
previously isolated under similar low-temperature,
hypersaline conditions (Amato & Christner, 2009;
Bakermans etal., 2006; Bowman etal., 1996), which
is a common environment for their growth. UTB113
represents the first isolation of P. cryohalolentis from
the Antarctic continent (Amato & Christner, 2009;
Bakermans etal., 2006; Goordial etal., 2013; Smith
et al., 2009). Bacterial diversity can occur in this
region, and there is a need to extend research to areas
with extreme environmental conditions.
The isolates were negative for oxidase and positive
for catalase and showed a positive reaction to nitrate
reduction. The latter promotes the analysis of isolated
bacteria based on nitrate acting as an electron accep-
tor, which is characteristic of the reduction of per-
chlorate (Bardiya & Bae, 2011; Sevda etal., 2018).
The genes responsible for nitrate reduction generally
coexist with those that reduce perchlorate because
of their similar potential to reduce nitrate to molecu-
lar nitrogen and perchlorate to chloride (Ucar etal.,
2017; Wan etal., 2017; Zhao etal., 2011).
Horseshoe Island
Bacteria isolated from Horseshoe Island were related
to I. loihiensis. This species was isolated for the first
time from a hydrothermal source of the submarine
Loihi volcano in Hawaii, at a depth of 1300m. Idi-
omarina loihiensis is a halophilic bacterium with an
optimum grow at temperatures of 4–50°C (Donachie,
2003). Thus, the marine ecosystem of Antarctica may
be one of their habitats. This genus was reported by
Malavenda et al. (2015), who isolated I. loihiensis
from Arctic and Antarctic sediments. Specifically,
this psychrotolerant bacterium was isolated from
hydrocarbon-amended microcosms containing crude
or diesel oil. Malavenda etal. (2015) demonstrated
the biosurfactant-production capability of Idiomarina
sp. 185 in cold environments. In addition, I. loihien-
sis was isolated from the Peruvian Andes under halo-
philic conditions (Castelán-Sánchez etal., 2019).
Half Moon Island
Bacteria isolated from Half Moon Island were
related to P. nivimaris, S. aquimarina and P. lactis.
The genus Psychrobacter was also isolated from
Deception Island, indicating the psychrophilic or
psychrotolerant behaviour of this genus. In addi-
tion, P. nivimaris has been isolated from hypersaline
environments and low temperatures in the Antarctic
Ocean (Yumoto etal., 2010). S. aquimarina is a fac-
ultative anaerobic bacterium isolated for the first time
in South Korea. In addition, this species has been
isolated from Antarctica and is resistant to extreme
conditions and low temperatures (Reddy etal., 2003;
Santos etal., 2015). Pseudomonas genera have been
isolated from different environments, even under
extreme conditions, owing to their versatile meta-
bolic mechanisms (Peix et al., 2018). However,
to the best of our knowledge, P. lactis is the first iso-
lated from this species in Antarctica.

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Sodium chloride and perchlorate susceptibility of the
bacterial isolates
Environmental factors such as salinity can influence
bacterial growth and inhibit metabolic activity as a
result of (i) increased osmotic stress on microorgan-
isms and (ii) altered solubility or sorption of toxic/
essential ions (Yan etal., 2015). However, some bac-
teria can adapt to low osmotic potential through salt-
in-cytoplasm and osmolyte accumulation mechanisms
(Long etal., 2018). The low availability of freshwater
in the Antarctic continent has led to the development of
salt tolerance mechanisms as a microbial survival strat-
egy (Aguila-Müller, 2015; Cowan etal., 2014; Zhang
etal., 2013). Therefore, the tolerance of the isolates in
our experiments to a NaCl concentration of 30% can
be attributed to the low availability of freshwater and
high salinity of the sampled ecosystem. Isolates related
to Psychrobacter, Idiomarina, Sporosarcina and Pseu-
domonas genera have been reported to be tolerant to
salinity, particularly those isolated in this study; there-
fore, they have an adaptive advantage (Azevedo etal.,
2013; Bakermans etal., 2006; Bowman et al., 1996).
The ability of the isolated species to tolerate an NaCl
concentration of 30% is promising for their use as a
biological system to reduce perchlorate in high salin-
ity ecosystems, where the presence of perchlorate has
been reported in numerous studies (Cang etal., 2004;
Chung et al., 2009; Martin et al., 2009; Ryu et al.,
2011; Singh & Jha, 2016).
Perchlorate contamination of marine sediment and
seawater, as well as other environmental matrices (for
example, Antarctic soil), has resulted in the stimula-
tion of bacterial growth and an increase in the number
of bacteria that can resist and degrade these pollutants
(Achenbach & Coates, 2004; Calderón et al., 2014,
2017; Jiang etal., 2016, 2020; Kounaves etal., 2010;
Nam etal., 2016). The dominant members of bacte-
rial communities that have been found to resist and
degrade perchlorate belong to the Alphaproteobac-
teria, Betaproteobacteria and Gammaproteobacteria
subclasses. The genera isolated in this study are part of
the Gammaproteobacteria subclass (Achenbach etal.,
2001; Carlström etal., 2016; Sevda et al., 2018; Zhu
et al., 2016). However, there are no previous reports
on the evaluation of perchlorate resistance in these
psychrophilic and psychrotolerant genera and species.
Our results confirmed that native Antarctic bacteria in
the sediment samples were tolerant to environmental
concentrations of perchlorate and can tolerate higher
concentrations up to 10,000 mg/L, even at low tem-
peratures. This factor can limit the degradation pro-
cess, given that perchlorate-reducing bacteria are more
efficient under mesophilic or thermophilic conditions
(Liebensteiner etal., 2015; Song etal., 2019).
Most perchlorate-reducing bacteria are anaerobic
and facultative, and molecular oxygen is produced
as an intermediate for microbial perchlorate reduc-
tion in a process that exudes nitrate (Bruce et al.,
1999; Sevda etal., 2018). Although these bacteria
undergo degradation processes in a wide range of
environmental conditions, for the low temperature,
high salinity environments of Antarctica, H. lacus-
profundi has been shown to tolerate elevated con-
centrations of highly oxidative perchlorate salts. In
addition, its enzyme (β-galactosidase) was able to
maintain its activity under these conditions, which
is a possible key mechanism for the stable activ-
ity of this microorganism (Correa & Abreu, 2020;
Laye & DasSarma, 2018). The isolates in this study
were negative for β-galactosidase. Further research
is required to understand the enzymatic activity of
the mechanisms related to the resistance and reduc-
tion of perchlorate. It is possible that some critical
anaerobic isolates were missed during the aerobic
treatment in this study; hence, additional experi-
ments should be carried out under anaerobic con-
ditions to enrich for active microorganisms that
may improve perchlorate degradation. These may
include the species isolated in this study, which are
found in a wide range of low-temperature habitats
and marine environments, including Antarctic ice,
soil and orogenic sediments (Bozal etal., 2003; Che
etal., 2013).
Evaluation of perchlorate reduction by isolates
A variety of perchlorate-reducing bacterial species
can reduce this contaminant; however, the percentage
of reduction varies according to genus and the period
of exposure to the pollutant. The rates of perchlorate
reduction determined in this study were comparable
to those reported by Acevedo-Barrioset al. (2019a), where
Nesiotobacter, Salinivibrio, Vibrio, Bacillus and
Staphylococcus genera were isolated from Caribbean
hypersaline soils, and reduced between 10 and 25% of
10,000mg/L of KClO4ˉ. In the present study, perchlo-
rate reduction was performed by P. cryohalolentis, P.

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urativorans, I. loihiensis, P. nivimaris, S. aquima-
rina and P. lactis, thus demonstrating their ability to
reduce this contaminant. However, further investiga-
tion is required to determine the optimum reduction
under different environmental conditions (e.g. tem-
perature and the presence/absence of electron accep-
tors/donors) (Chaudhuri etal., 2002).
Additionally, the bacteria isolated in this study
can be used together or mixed with other cultures to
enhance the bioremediation process through sym-
biotic interactions. For example, Kucharzyk et al.
(2013) reported that the rate of perchlorate reduc-
tion increased 2.06-fold and 4.08-fold when using
consortia in comparison to the use of isolated bacte-
ria. In addition, Nor etal. (2011) found that perchlo-
rate-reducing cultures could treat high perchlorate
concentrations.
Conclusion
This study confirmed that native Antarctic bacte-
ria isolated from sediment samples were tolerant to
environmental concentrations of perchlorate and can
tolerate higher concentrations of up to 10 000mg/L.
P. cryohalolentis and P. urativorans were isolated
from Deception Island; I. loihiensis from Horseshoe
Island and P. nivimaris, P. lactis and S. aquimarina
from Half Moon Island. Only a few studies have
reported on the reduction of perchlorate by Antarc-
tic microorganisms, our findings demonstrated that
these isolated bacteria can reduce KClO4ˉ, with
reduction between 21.6 and 40%, thus providing a
possibility for biotechnology and the treatment of
areas polluted by perchlorate. I. loihiensis was the
bacterium with the highest reduction in perchlo-
rate, while P. lactis presented the lowest reduction.
In addition, the isolates are capable of growing in
a culture medium with a high NaCl concentration;
therefore, they are halophilic or halotolerant. This
salinity tolerance is promising for use as a biological
system to reduce perchlorate in high-salinity eco-
systems. It should be noted that there are no previ-
ous reports on the isolation of P. cryohalolentis and
P. lactis from the Antarctic continent. Therefore,
this study expands the existing knowledge regard-
ing the presence of perchlorate-reducing bacteria in
Antarctica.
Acknowledgements The authors thank the Directorate of
Research at the Universidad Tecnológica de Bolívar for financ-
ing this project. They also thank the Colombian Ocean Com-
mission coordinator of the Colombian Antarctic Program,
Spanish Polar Committee-CPE, Spanish Navy, and Spanish
Oceanographic Ship BIO Hespérides A-33 for providing logis-
tic support for the displacement and sampling of different evalu-
ation points in Antarctica. The authors also thank Sandra Baena
of the Pontificia Universidad Javeriana and Carolina Díaz Card-
enas for their support with the molecular analysis of the isolates.
Funding This research was supported by the Research, Inno-
vation, and Entrepreneurship Directorate of the Technological
University of Bolivar.
Availability of data and materials The datasets gener-
ated and/or analysed during the current study are available
in the GenBank repository with code numbers MW130840,
MW130841, MZ420735, MZ420736, MZ420737, MZ420738
and MZ420739.
Declarations
Conflict of interests The authors declare no competing in-
terests.
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