The Vigor, Futility, and

Application of Microbial
Element Cycles in Alkaline
Soda Lakes
A beaker containing a
microbial mat from an
alkaline soda lake. Who
Marianne Haines1, Varada Khot1, and Marc Strous1 resides within and to what
future applications might
they give rise?
1811-5209/23/0019-030$2.50  DOI: 10.2138/gselements.19.1.30

A
lkaline soda lakes are known as some of nature’s most biologically and sodium concentrations drives
productive ecosystems. Vigorous production (photosynthetic conver- interest from both fundamental
and applied perspectives. This
sion of inorganic carbon into biomass) is countered by incremental work explores biomass produc-
biomass degradation, which fuels and feeds a diverse microbial community. tion and breakdown in alkaline
Learn here about key adaptations that help microbes survive and thrive in soda lakes and features intriguing
uses of their microbial inhabitants
the extreme conditions of alkaline soda lakes. Dive into the interconnected in society (packaged in ‘Boxes’
microbial element cycles of alkaline soda lakes and discover how the geochem- throughout this article).
istry of these environments presents microbes with unique challenges and
opportunities. Throughout this article, explore how the microbial inhabitants KEY MICROBIAL
ADAPTATIONS
of alkaline soda lakes have been harnessed in biotechnological applications,
High carbonate and sodium
including the production of protein-rich food, detergent enzymes, and the concentrations present unique
purification of biogas. challenges to life—challenges that
Keywords: alkaline soda lake; geomicrobiology; biogeochemistry; have been overcome by alkaline
applied environmental microbiology; alkaliphile soda lake microbes. Microbes
adapted to high pH (9+) are dubbed
‘alkaliphiles’. Those specifically
INTRODUCTION accustomed to life in sodium carbonate brines are ‘natrono-
Despite their extreme chemistry, high salt concentrations, philes’ or ‘soda-loving’ (Sorokin 2017). To date, natrono-
and high pH, alkaline soda (Na–HCO3–CO3) lakes are very phile research has dealt almost exclusively with bacteria
active biological ecosystems. Alkaline soda lakes are home and archaea—thus they are the spotlight of this article.
to many. On a microscopic scale, bacteria, archaea, viruses,
Numerous microbes collected from alkaline soda lakes
and microbial eukaryotes thrive. Small brine shrimp and
have been isolated, grown, characterised, and identified
brine flies are common. In some lakes, dense populations
in the laboratory. These are collectively known as ‘culture-
of cyanobacteria feed large flocks of flamingos. Although
dependent’ approaches. DNA sequencing of entire alkaline
plants are scarce, photosynthesis is in full force.
soda lake microbial communities has revealed even
Vigorous oxygenic photosynthesis by cyanobacteria and more species. This is an example of a ‘culture-indepen-
microalgae lead to some of the world’s highest rates of dent’ approach (Antony et al. 2013; Sorokin et al. 2014;
carbon fixation and growth (Melack and Kilham 1974). Yet, Vavourakis et al. 2016; Zorz et al. 2019). Unsurprisingly,
primary production fuels an active biological food chain. alkaline soda lake microbes differ from their freshwater
Thus, high gross productivity does not necessarily translate and marine relatives.
into high net productivity. Microbial element cycling in
Compared with pH-neutral microbes, natronophiles
alkaline soda lakes is to some extent futile, a fascinating
contend with different chemiosmotic gradients. All living
network of diverse metabolisms producing little perma-
cells have an ion gradient across their membrane that
nent change.
they use to drive molecule transport, cell mobility, and
The microbiology of alkaline soda lakes has been an intense regeneration of the energy carrier adenosine triphosphate
and successful area of study. Alkaline soda lake microbes (ATP). At neutral pH, protons (H+) are integral to this
are implicated in the biogeochemical cycling of carbon, gradient with cells having a higher internal pH than their
nitrogen, sulfur, iron, phosphorous, and other elements. surroundings. Natronophiles have the same internal pH as
Almost all microbial metabolisms known at neutral pH microbes living at neutral pH, but this pH is lower than their
have been described in alkaline soda lakes, although surroundings. For natronophiles, the ion gradient instead
their geochemistry appears to favour some metabolisms consists mainly of sodium, which has a high external and
while hindering others. Alkaline soda lakes present unique low internal concentration (Sorokin 2017). From an evolu-
challenges and opportunities to life. Understanding how tionary perspective, this requires changes or additional
microbes contend with high pH, carbonate alkalinity, modules to many ion-transport enzymes. Adaptions to
high sodium concentrations are also present in marine
microbes. In both ecosystems, high ion concentrations
1 Department of Geoscience require additional work for cells to balance osmotic forces
University of Calgary across the cell membrane.
Calgary, Alberta, Canada
E-mail: [email protected]
E-mail: [email protected]
E-mail: [email protected]

E lements , V ol . 19, pp. 30–36 30 F ebruary 2023

Because of inorganic carbon speciation at high pH, Microbially catalysed oxidation and reduction, as well as
natronophiles must also contend with extremely low CO2 the uptake and release of inorganic and organic molecules,
concentrations. Yet the primary productivity of alkaline creates biologically mediated elemental cycles. Many
soda lakes relies on photosynthesis—a process that requires related natronophilic microbes harbouring similar metab-
CO2 . To combat this, alkaline soda lake cyanobacteria use olisms have been found in alkaline soda lakes separated by
a ‘carbon-concentrating mechanism’ (CCM). Bicarbonate large geographical distances (Antony et al. 2013; Sorokin
is transported across the cell membrane and, once inside, 2017; Zorz et al. 2019). The microbes highlighted in this
is split by the enzyme carbonic anhydrase to yield CO2 . article are common inhabitants of alkaline soda lakes.
Carbon dioxide is concentrated in the vicinity of rubisco—
the enzyme that creates the first organic carbon molecule. Carbon Cycling
This CCM also occurs in marine cyanobacteria. At pH 8, For phototrophs, like cyanobacteria and microalgae, light
seawater contains a greater relative proportion of CO2 than availability is paramount. Depending on lake conditions
alkaline soda lakes, but bicarbonate is still by far the most (particularly the depth of light penetration), phototrophs
abundant form of inorganic carbon. Thus, both for marine may form biofilms on the surface, be suspended in the
and alkaline soda lake cyanobacteria, the CCM is critical water column, or reside at the sediment–water interface
in converting the large pool of available inorganic carbon (Fig. 1A). Phototrophs uptake bicarbonate and create a
into CO2 . locally oxic zone. In alkaline soda lakes, cyanobacteria
(Fig. 2) are responsible for most productivity. Arthospira,
MICROBIAL ELEMENT CYCLING Spirulina (Box 1), Nostocales, Phormidium, and Nodosilinea
Let us start our journey with an overview that explains how are common, as are the microalgae Dunaliella, which can
microbes behave in alkaline soda lakes—which elements bloom when the salinity (g/L) increases (Fig. 1B) (Sorokin
do they use and for what? The microbial element cycles et al. 2014; Zorz et al. 2019). To fulfil their energy needs in
comprise a series of reactions that build and break down the dark, oxygenic phototrophs catabolise internal energy
biomass. To build biomass, ‘autotrophs’ (organisms that storage compounds via aerobic respiration if oxygen is
produce their own food from sunlight, water, CO2 , or available or via fermentation in the absence of oxygen.
other chemicals) and ‘heterotrophs’ (organisms that eat
other plants, animals, or microbes for energy and nutri- A B
ents) use inorganic and organic carbon, respectively. To
power cell growth and maintenance, microbes use sunlight
and/or chemical energy. Chemical energy is acquired
when microbes couple the oxidation of one molecule (the
electron donor) to the reduction of another (the electron
acceptor). A huge array of organic and inorganic electron
donors are used by microbes. Most electron acceptors are
inorganic.
Cyanobacteria and microalgae (‘phototrophs’—organ-
isms that use energy from sunlight to synthesize organic
compounds for nutrition) feed and power a diverse commu-
nity of microbes in alkaline soda lakes. Sunlight, water,
and inorganic carbon are converted via photosynthesis to Microbial communities of alkaline soda lakes.
Figure 1
biomass and oxygen. While biomass sinks, oxygen bubbles (A) Phototrophic microbial mat collected from
rise. As we travel down the water column, oxygen avail- alkaline soda lakes on the Cariboo Plateau, Canada. Photo
courtesy of Yihua Liu. (B) Micrograph of oxygenic phototrophs,
ability wanes as a result of outgassing and the degradation primarily filamentous cyanobacteria, from Goodenough Lake,
of sinking biomass by aerobic respiration. Canada. Photo: Marianne Haines.
During aerobic respiration, oxygen is used as the electron
acceptor. Once oxygen is depleted, microbes gain energy
via anaerobic respiration by reducing other oxidised B ox 1 SPIRULINA
compounds like nitrate, ferric iron, and sulfate. When a For many, alkaline soda lakes are a food source.
single organic substrate serves both as the electron donor In African countries, Spirulina are collected from
and acceptor, this is known as fermentation. Fermentation natural lakes and dried into cakes called dihé (Habib
generates partially oxidised by-products like acetate and et al. 2008). Spirulina are nutritious and protein-rich
formate. Microbial activity creates chemical gradients in (60%–70% of dry weight) (Habib et al. 2008). Their
stagnant water, sediments, and microbial aggregates (like large-scale commercial production as a food and
microbial mats and biofilms). Microbes occupy different nutritional supplement began in the 1970s. Today,
locations along such gradients depending on their lifestyle. many companies produce Spirulina outdoors in
For example, oxygen may be toxic to microbe A but essen- warm climates in open hectare-scale raceway ponds
tial to microbe B. Microbes exhibit exceptional metabolic (Habib et al. 2008; Lu et al. 2011). The chemistry
flexibility and can switch substrates based on availability. of these ponds is important to their commer-
Microbes use energy gained from oxidation and reduction cial success. At production facilities, Spirulina are
to transport and assimilate elements from the environment typically grown around pH 9 with an alkalinity of
into macromolecules including carbohydrates, proteins, 150 mEq, conferred by sodium bicarbonate (Habib
lipids, and nucleic acid (DNA and RNA). These biomolecules et al. 2008). These conditions resemble those of
contain carbon, nitrogen, phosphorus, sulfur, and a variety alkaline soda lakes and help exclude predators
of transition metals like iron. In aquatic environments, the (which might eat the cyanobacteria) and competi-
growth of primary producers is typically limited by the tors (which might replace the cyanobacteria).
availability of nitrogen, phosphorous, or iron. Spirulina are harvested, dewatered, and sold in many
forms—intact cells are sold fresh, dried to powder/
cake, or compacted into pills.

E lements 31 F ebruary 2023

 Microbial element cycling in alkaline soda lakes.
Figure 2
A simplified overview of microbial element cycling in B ox 2 STAIN REMOVAL IN THE LAUNDRY INDUSTRY
alkaline soda lakes with example taxa. Chemical gradients can
change at the millimetre scale, influenced by, for example, water Laundry detergent used to be just soap. Today, a
column mixing and the action of microbial metabolism. Microbial diversity of added enzymes enhance their cleaning
element cycling is extremely interconnected. Depending on performance (Contesini et al. 2018). Enzymes target
availability, a single microbe may (or may not) use sunlight, switch
between electron donors and acceptors, or partake in fermentation different types of grime. Common additives include
when required. proteases (e.g., for blood), lipases (e.g., for animal
fat), amylases (e.g., for starchy baby food), mannases
In oxygen-depleted zones, a different flavour of photosyn- (e.g., for gelling agents in mayonnaise), pectinases
thesis occurs; ‘anoxygenic’ phototrophs use light and can (e.g., for fruit jam), and cellulases (Bora et al. 2013).
fix CO2 but use electron donors like sulfide and hydrogen Cellulases degrade the cellulose in, for example,
(as H 2) for CO2 reduction instead of water, and thus, do pilling cotton, releasing dirt and keeping clothing
not produce oxygen. For example, ‘purple sulfur bacteria’ smooth. Laundry enzymes contend with three
(visible to the naked eye as a purple layer in microbial mats) challenges: they must (1) function in the presence
of the order Chromatiales gain electrons from sulfide oxida- of other detergent ingredients like surfactants and
tion for carbon fixation (Sorokin et al. 2014; Vavourakis et chelating agents; (2) withstand the temperature of a
al. 2016). Other common phototrophic microbes include wash cycle (hot or cold); and (3) be stable at high pH
the family Rhodobacteraceae and members of the class (laundry detergent pH ranges from 9 to 12) (Ibrahim
Gemmatimonadetes (Fig. 2)—whose capacity to use light et al. 2015). Proteases prospected from Bacillus
energy has only recently been discovered (Sorokin et al. species from Egyptian alkaline soda lakes were the
2015; Vavourakis et al. 2016; Zorz et al. 2019). first enzymes added to laundry detergents in the
1950s (Contesini et al. 2018). Given the high pH of
The death of phototrophs releases diverse lipids, sugars, laundry detergent, alkaline soda lakes are prime
proteins, and nucleic acids like DNA. These are taken up by ecosystems to search for novel laundry enzymes. By
heterotrophs and used both as energy sources and supplies most accounts, the laundry detergent market is the
of carbon, nitrogen, sulfur, etc. To break down large biomol- largest consumer of high-pH enzymes, especially
ecules into smaller moieties that can be imported into their proteases (Contesini et al. 2018).
cells, heterotrophs secrete various enzymes. These enzymes
include proteases (digest proteins); lipases (deconstruct
lipids); amylases, cellulases, and pectinases (depolymerise
polysaccharides); and more. Because enzymes are secreted Such enzymes are of industrial value (Fig. 3) because they
or exposed on the cell surface, they must be stable and perform specific reactions under ‘extreme’ conditions.
active at high pH and in Na–HCO3–CO3 brines. High-pH enzymes are sold commercially for use in laundry
detergents (Box 2), the pulp and paper industry (Box 3), and
the leather making process (Box 4). Enzymes can enhance
the sustainability of these applications when they replace
or reduce the use of aggressive chemicals (Wang et al. 2017;
Khambhaty 2020). Additionally, the development of effec-
tive enzymatic cold water laundry detergents saves energy
otherwise required for heating water (Contesini et al. 2018).

E lements 32 F ebruary 2023

 In the absence of oxygen, heterotrophs use other electron
B ox 3 PULP AND PAPER
acceptors, discussed in subsequent sections of this text,
The raw material for paper, ‘lignocellulosic’ plant including nitrate, ferric iron, and sulfate. These are used in
biomass, contains cellulose, hemicellulose, and a thermodynamically determined order. Fermentation of
lignin; together these carbohydrates provide struc- organic carbon also yields energy. For example, Natronincola
tural integrity to plant cell walls. Plant biomass and Tindallia species ferment remnants of proteins (Fig. 2)
is ‘pulped’ to separate lignin and hemicellulose (Sorokin 2017).
from the desired cellulose. A common method,
Fermentation products, like acetate and H 2, are converted
Kraft pulping, produces a pulp with some residual
to methane by microbes in the sediment or within anoxic
lignin. Lignin confers an undesirable colour to the
pockets of suspended particles (Nolla-Ardèvol et al. 2012;
pulp (Roncero et al. 2005). Traditionally, paper
Porsch et al. 2015; Sorokin 2017; Fazi et al. 2021). This
whitening is achieved by removing lignin via
process is known as methanogenesis and is exploited
chlorine bleaching, but this generates toxic and
industrially to produce biogas from waste by anaerobic
polluting organochlorines. Xylanase enzymes can
digestion (Box 5). For microbes, there is more than one
be used as a pre-treatment to reduce chlorine use
way to produce methane. In alkaline soda lakes, archaea
(Roncero et al. 2005). Xylanases are thought to assist
like Methanolobus and Methanosalsum produce methane
bleaching by (1) breaking hemicellulose–lignin
from methylated compounds like methanol (Nolla-
bonds, thereby freeing lignin, and (2) cleaning
Ardèvol et al. 2012; Sorokin et al. 2014; Sorokin 2017).
up crystallised xylan on the fibre surface. Both
Methanocalculus can generate methane by reducing CO2
mechanisms increase the accessibility of bleaching
with H 2 or formate as electron donors (Sorokin 2017; Fazi
reagents (Roncero et al. 2005). Because the Kraft
et al. 2021). Alternatively, Methanosaeta ferments acetate to
pulping process degrades plant biomass in hot water
methane and CO2 (Fig. 2) (Sorokin 2017; Fazi et al. 2021).
at high pH, durable enzymes are required (Wang
When oxygen is available, methanotrophic bacteria like
et al. 2017). A xylanase-producing Alkalibacterium
Methylomicrobium oxidise methane back to CO2 (Fig. 2)
was isolated from alkaline soda lakes in China. The
(Antony et al. 2013; Sorokin et al. 2014). In Lake Sonachi
xylanase, active at pH 9 and 55 °C was transferred to
in the East African Rift Valley, pelagic methanogenesis
fast-growing Escherichia coli by genetic modification
causes surface waters to accumulate high concentrations
(Fig. 3) (Wang et al. 2017). High-pH xylanases for
of biogenic methane (Fazi et al. 2021). It follows that
the pulp and paper industry are sold commercially.
lakes may emit what was once fixed organic carbon to the
atmosphere as methane.

B ox 4 LEATHER PROCESSING
HIGH-pH ANAEROBIC DIGESTION OF
Multiple high-pH steps in leather making are B ox 5 BIOMASS FOR BIOENERGY
aided by microbial enzymes (Khambhaty 2020).
Anaerobic digestion is a microbial process used
High-pH proteases, lipases, and amylases assist
extensively to recover energy as biogas, a mixture
hide preparation by degrading surface grime like
of methane and CO2, from organic waste. Usually,
grease and blood, and components within the hide
industrial anaerobic digestion occurs at neutral
like hyaluronic acid and plasma proteins (Bora
pH. For difficult-to-digest wastes like lignocellu-
et al. 2013; Khambhaty 2020). Leather making
losic plant material (e.g., wheat straw), high-pH
highlights the importance of enzyme specificity—
pre-treatment can help commence the breakdown
enzymes should have low activity against collagen,
process (Porsch et al. 2015). However, this means
leather’s essential structural protein (Zhou et al.
that waste must be thoroughly washed prior to
2018). Traditionally, hair or fur is removed chemi-
digestion, adding unit operations and compro-
cally using lime and sulfide. Unfortunately, these
mising sustainability. This underscores the benefit
chemicals generate a polluting sludge and are detri-
of developing an industrial high-pH digestion
mental to leather workers’ health. Proteases loosen
process. Advantageously, high-pH digestion would
the hair root structure, improving sustainability
also enable the production of pure methane because
and safety (Khambhaty 2020). Alkaline soda lakes
the CO2 fraction of the biogas would remain in
have been bioprospected for enzymes applicable
solution. Presently, the technology is still under
to the leather industry. For example, E. coli was
development—ammonia toxicity at high pH
genetically modified to excrete a protease from an
remains a challenge (Nolla-Ardèvol et al. 2012;
Idiomarina species isolated from a Chinese alkaline
Sorokin 2017). High-pH anaerobic digestion has
soda lake (Zhou et al. 2018). The enzyme displayed
been trialled with sediments from various alkaline
optimal activity at pH 10, and effectively dehaired
soda lakes as a source of microbes (Nolla-Ardèvol et
cattle hide and goat-, pig-, and rabbit-skins. Today,
al. 2012; Porsch et al. 2015).
many commercial high-pH enzymes are available
for various leather-making steps.
Nitrogen Cycling
For every five carbon atoms assimilated, microbes need
In their natural context, enzymes help release energy and
about one nitrogen atom. Nitrogen, as ammonia, nitrate,
nutrients bound up in biomolecules, profiting hetero-
nitrite, or urea, is often a limiting nutrient in aqueous
trophs. Aerobic heterotrophs pair biomolecule degradation
environments. Alkaline soda lakes contain variable, but
with oxygen reduction. This liberates chemical energy and
mostly low, nitrogen concentrations. In alkaline soda lakes
organic material, which is used as cellular building blocks.
on the Cariboo Plateau, ammonia and nitrate are undetect-
In alkaline soda lakes, Halomonas and Wenzhouxiangella
able (Zorz et al. 2019). Melack et al. (1982) also reported
(Fig. 2) (Sorokin et al. 2014; Vavourakis et al. 2016; Zorz et
low concentrations of inorganic nitrogen in alkaline soda
al. 2019) live near cyanobacteria and microalgae, exploiting
lakes in the East African Rift Valley. Ammonia is detectable
both the released organic carbon and the produced oxygen.
in lakes in the Russian Altai region, but nitrate remains

E lements 33 F ebruary 2023

 A

B C
EF E

Path from enzyme discovery to production. found that grow well on these molecules, the target enzymes may
Figure 3
(A) To discover a new enzyme that converts a target be separated from the cells for further tests. If successful, the gene
class of molecules, researchers ‘bioprospect’ an environment with responsible for encoding the novel high-performing enzyme may
chemistry as the target process. (B) The material collected contains be transferred into different, fast-growing microbes. (E) Enzymes
a microbial community. (C) Typically, the community is exposed to can be produced at scale by growing microbes in large bioreactors
the target substrate(s) in the lab. Microbes that naturally produce or ‘fermenters’. (F) Finally, enzymes are sold as granules or in
the desired enzyme are enriched. (D) Once microbes have been liquid form.

low (Samylina et al. 2019). Apparently, India’s Lonar Lake NH3) and sodium (>1 M Na+) concentrations (Sorokin and
is an outlier boasting a comparatively high (2.4 mg·L−1) Kuenen 2005a). The second step, nitrite oxidation, appears
concentration of nitrate (Antony et al. 2013). to be more robust—Nitrobacter species are easier to isolate
from alkaline soda lakes. Nitrite oxidisers may be favoured
The presence and expression of genes involved in N2
by reduced nitrite toxicity at high pH. Under neutral pH
fixation in many natronophiles, as well as field and labora-
conditions, nitrite exists partially as undissociated nitric
tory measurements of acetylene reduction rates (a proxy
acid, but at high pH, its concentration is low (Sorokin and
measurement for N2 fixation), suggest some microbes can
Kuenen 2005a).
collect their own nitrogen from the atmosphere (Sorokin
et al. 2014; Samylina et al. 2019; Zorz et al. 2019). Nitrogen- The produced nitrate can be used as an electron acceptor
fixers in alkaline soda lakes include cyanobacteria, anoxy- and reduced partially or fully to N2 (denitrification) by,
genic phototrophs, sulfate reducers, and fermentative for example, heterotrophic Halomonas species or autotro-
Firmicutes (Sorokin et al. 2014; Zorz et al. 2019). Salinity phic Thioalkalivibrio (Fig. 2) (Sorokin et al. 2015). Nitrate
(g·L−1) appears to control which populations of N2-fixers are may also be converted to ammonia in a process known
active (Samylina et al. 2019). Nitrogen fixation is a bioen- as dissimilatory nitrate reduction to ammonia (DNRA)
ergetically costly process only used when other forms of (Sorokin 2017). In a study of Canadian alkaline soda lakes,
nitrogen limit growth. genes for denitrification were not found. DNRA genes were
present but were not detected in the proteome and thus
When heterotrophs break down nitrogen-rich organic
were apparently unused (Zorz et al. 2019). Laboratory
matter, like amino acids, excess nitrogen is released to the
studies have demonstrated active DRNA, but the extent to
environment as ammonia. This leads to a challenge at high
which this occurs in situ is unknown (Sorokin et al. 2015).
pH as ammonium exists in part as toxic ammonia (NH3)
(Sorokin and Kuenen 2005a; Nolla-Ardèvol et al. 2012). The nitrogen cycle in alkaline soda lakes is in part controlled
Uncharged ammonia diffuses through cell membranes and, by salinity. Salinity gradients influence which N2-fixers are
as a base, raises the cell’s internal pH. Higher internal pH, active, and high sodium concentrations appear to restrict
an increase in maintenance energy, and enzyme inhibition nitrification (and thus perhaps the nitrogen cycle more
are proposed mechanisms for ammonia toxicity. At high generally) (Sorokin and Kuenen 2005a; Samylina et al.
pH, nitrogen can be lost from lakes via ammonia volatilisa- 2019). The nitrogen cycle of alkaline soda lakes remains
tion (Jellison et al. 1993). an exciting topic for future research.
Nitrification by aerobic microbes like Nitrosomonas and
Sulfur Cycling
Nitrobacter (Fig. 2) (Sorokin and Kuenen 2005a) oxidises
ammonia to nitrite, and subsequently nitrate, to yield Microbes assimilate about 1 sulfur atom for every 20 carbon
energy. The first step, ammonia oxidation, has been detected atoms. Sulfur is incorporated into cellular components, like
in Mono Lake and Big Soda Lake in the US. However, the the amino acids cysteine and methionine. Some microbes
process may be inhibited at higher ammonia (>4 mM also rely heavily on sulfur compounds to acquire chemical

E lements 34 F ebruary 2023

energy. Sulfur-metabolising microbes have been identified
B ox 6 HYDROGEN SULFIDE REMOVAL FROM GAS
in numerous alkaline soda lakes and studied extensively
(Sorokin and Kuenen 2005b; Sorokin et al. 2011). Likely, Both natural gas and biogas contain methane,
they are more active in Na–HCO3–CO3–SO4 brines, e.g., CO2, and hydrogen sulfide (H 2 S). Hydrogen sulfide
Mono Lake (USA), as opposed to low-sulfate brines, e.g., is corrosive, toxic, and flammable. It must be
Lonar Lake (India). In alkaline soda lakes, high pH creates removed before gas can be combusted. A solution
distinctive sulfur chemistry. that contains 0.5–1 M sodium bicarbonate at pH
8.2–9, conditions reminiscent of alkaline soda
At high pH, hydrogen sulfide dissociates to the non-volatile
lakes, effectively absorbs H 2 S from gas streams
bisulfide ion (HS−), reducing sulfide toxicity. At neutral
(Sorokin et al. 2013). At high pH, H2S gas reacts with
pH, volatile hydrogen sulfide diffuses through the cell
OH− to produce bisulfide (HS−). This is the first step
membrane and inhibits aerobic respiration. Hydrogen
in the commercial ‘Thiopaq’ process (Driessen et al.
sulfide gas dissolves well at high pH and high carbonate
2011) to purify gas streams. The now sulfide-rich
alkalinity, enabling the successful development of desul-
solution enters a bioreactor containing sulfide-
furisation biotechnology (Box 6). Elemental sulfur reacts
oxidising bacteria. These bacteria oxidise bisulfide
abiotically with sulfide to form polysulfides (chains of
to elemental sulfur while growing as biofilms on
sulfur atoms), which are stable only at high pH and repre-
support media. Microbes related to those found
sent a unique form of bioavailable sulfur in alkaline soda
in alkaline soda lakes, like Thioalkalivibrio, are
lakes (Sorokin and Kuenen 2005b). At neutral pH, micro-
enriched in Thiopaq bioreactors (Sorokin et al.
bial sulfide oxidation can acidify the environment, but in
2015). Elemental sulfur is separated by gravity
alkaline soda lakes, sulfuric acid is neutralised by the strong
settling and can be used as a fungicide or fertiliser.
buffering capacity of the brine.
For small- to mid-scale gas streams, the Thiopaq
Aerobic or oxygen-tolerant microbes that oxidise sulfur process is more economical than typical chemical
compounds can be abundant in surface sediments, desulfurisation methods. The Thiopaq process was
converting sulfide to thiosulfate (S2O32−) or sulfate (Sorokin first applied at full scale to treat biogas from the
et al. 2011). Members of the genus Thioalkalivibrio are anaerobic digestion of paper mill effluent in 1993
apparently the most widespread with >100 different (Driessen et al. 2011) and is now used worldwide.
isolated variants (Fig. 2). Anaerobic phototrophic ‘purple
sulfur bacteria’, including Ectothiorhodospira, are also very
common (Driessen et al. 2011; Sorokin et al. 2014; Zorz
magnetite (an iron (II/III) oxide) and siderite (iron (II)
et al. 2019).
carbonate), have been isolated from lakes in southern
Alkaline soda lakes are also home to anaerobic microbes Siberia and Lake Magadi in Kenya (Sorokin 2017; Zavarzina
that reduce diverse sulfur compounds including sulfate, et al. 2020). Recent work has shown that G. ferrihydriticus
sulfite, thiosulfate, and polysulfides (Sorokin et al. 2014). can also oxidise siderite while reducing carbonate to
Complete reduction, ‘sulfidogenesis’, produces hydrogen acetate (Zavarzina et al. 2020). Otherwise, Fe(II)-oxidising
sulfide (H 2 S). At neutral or acidic pH, sulfidogenesis can microbes, which are abundant in pH neutral and acidic
be restricted by product inhibition, e.g., when H2 S is not anoxic environments, remain elusive.
biologically/chemically oxidised or precipitated as FeS by
ferric iron. At high pH, H 2 S concentrations remain low, Phosphorous Cycling
favouring sulfidogenesis (Sorokin 2017). Desulfonatronum Microbes generally assimilate about 1 mole of phospho-
and Desulfonatrovibrio are common alkaline soda lake rous for every 100–200 moles of carbon. Phosphorous is an
residents with flexible sulfur-based metabolisms (Fig. 2; essential constituent of biomolecules (like DNA, lipids, and
Sorokin 2017). Microbes that reduce sulfur compounds ATP). Dissolved inorganic phosphate is generally believed
include autotrophic and heterotrophic species (Sorokin et to be more bioavailable than dissolved organic phosphate
al. 2011). (DOP)—an accumulation of DOP in the ocean indicates
that recycling within the food chain is restricted. In marine
Iron Cycling and freshwaters, phosphate regularly limits growth.
Some transition metals, such as iron and manganese, are
In alkaline soda lakes, recent work has suggested that
used by microbes as electron sources and sinks to acquire
enhanced access to inorganic phosphate may contribute
energy. Many more, such as copper, nickel, and cobalt, are
to the exceptional productivity of these lakes (Toner and
used as key components of enzymes. Although microbes
Catling 2020). A positive relationship between dissolved
use small amounts of transition metals relative to C, N, P,
inorganic carbon and the phosphorous concentra-
and S, they are essential to cell function. Here, we discuss
tion has been observed for carbonate-rich lakes. This
the availability and uptake of one such transition metal
phenomenon is explained by the sequestration of Ca 2+
used by almost all microbes: iron. Although iron is one of
in carbonate minerals, thereby limiting the formation of
the most abundant metals in the Earth’s crust, the unique
apatite (calcium phosphate minerals) and enabling higher
geochemistry of alkaline soda lakes renders collecting
dissolved phosphate (Toner and Catling 2020). Extremely
and exploiting Fe a tricky microbial feat. At the high pH
high (4 mM) phosphate concentrations are common in
of alkaline soda lakes, iron exists primarily within insol-
Last Chance Lake, Canada (Zorz et al. 2019; Toner and
uble Fe(III) minerals (Sorokin 2017). To access iron, some
Catling 2020). Even so, many alkaline soda lakes have low
microbes produce extracellular iron-chelating ‘sidero-
phosphate concentrations, likely the result of spatial and
phores’, complex organic molecules that reversibly bind
temporal differences in biological uptake rates, precipita-
iron ions. Siderophore production has been reported for a
tion, and source water supply. Early nutrient amendment
Halomonas species isolated from Soap Lake in Washington
studies in African alkaline soda lakes show that phosphate
State, USA (Figueroa et al. 2015). Microbes may also grow
does limit productivity (Melack et al. 1982). To date, micro-
on the surfaces of iron minerals.
bial phosphate cycling in these environments has not
Iron-reducing microbes, like Natronincola species and received much attention, leaving an interesting gap for
Geoalkalibacter ferrihydriticus, capable of reducing chelated future research.
Fe(III) and amorphous Fe(III) hydroxide to minerals like

E lements 35 F ebruary 2023

CONCLUSIONS ACKNOWLEDGMENTS
Alkaline soda lakes display amazing effectiveness in trans- We thank the reviewers and editors who donated their
forming sunlight energy into electron and element flows. time to the improvement of this work. This work was
Phototrophs fix organic carbon into biomass, which in turn funded by the Natural Sciences and Engineering Research
supports the growth and reproduction of diverse commu- Council, the Canada Foundation for Innovation, the
nity members. During biomass degradation, fixed organic Canada First Research Excellence Fund, Western Economic
carbon is transformed back to inorganic carbon. Among Diversification, Alberta Innovates, the General Sir John
microbes, natronophiles are uniquely suited to high pH Monash Foundation, the Government of Alberta, and the
and to high carbonate and sodium concentrations. In University of Calgary.
society, alkaline soda lake microbes can be harnessed to
generate products and drive chemical transformations.
Such microbes have already sparked many successful appli-
cations (see Boxes 1–6) as sources of protein-rich food,
pools of robust enzymes, and reservoirs of metabolisms
fit for industrial bioreactors. Likely, their contribution to
the bioeconomy is only just beginning.

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