water for microbial life. Microorganisms are also squeezed into these salty veins,
along with nutrients, for example, as seen in sea ice (Junge et al. 2004). Indeed,
halotolerance seems to be a phenotypic trait shared by all psychrophilic organisms
isolated to date. At sufficiently low temperatures, even highly concentrated brines
may freeze to a mere film of water adsorbed to mineral particles. This is a condition
where life is likely operating at the limits and activity is questionable. Additionally,
the nature of the salts present also plays a role in microbial survival, as differing salts
have different freezing points as well as different disordering properties which may
be disruptive to cells (Hallsworth et al. 2007; Pontefract et al. 2017). As a result of
understanding the added physiological stresses of sub-zero temperatures, the term
cryophile is increasingly being used to denote organisms that grow at sub-zero
temperatures, as opposed to psychrophiles, defined as having growth optima at
temperatures between 5
C and 15
C (Raymond-Bouchard et al. 2018; Cavicchioli
2006; Seckbach 2013).
Sub-zero growth has been observed in microorganisms with broad phylogenic
distribution and in all three domains of life. The current record for bacterial cellular
division at low temperature is À15
C by Planococcus halocryophilus OR1, a
bacterium isolated from Arctic active-layer soils (the top layer above permafrost
that thaws seasonally in the summer) (Mykytczuk et al. 2013; Raymond-Bouchard
and Whyte 2017). Other examples include Methanococcoides burtonii, an Archaeal
methanogen isolated from Ace Lake, Antarctica, and that can divide at À2.5
C
(Williams et al. 2011), and Rhodotorula glutinis FMT157, a yeast isolated from
spoiled commercial frozen peas and that can grow at À18
C (Collins and Buick
1989). This latter frozen pea isolate hints to a potentially overlooked aspect of
low-temperature microbiology—that psychrophilic microorganisms may be more
abundant and ubiquitous than expected. While most psychrophilic organisms have
been isolated from polar environments considered by humans to be relatively
“extreme”, much of the northern hemisphere that is densely populated by humans
(e.g. the cities of Toronto, or Montreal) undergoes a deep freeze regularly, encountering sub-zero temperatures for 4–6 months. It is quite probable that psychrotolerant
or possibly even psychrophilic organisms exist in the many northern environmental
niches that humans would not consider “extreme.” These examples of sub-zero
replication are known from isolated microbial cultures grown in laboratories. However as the vast majority of microorganisms cannot yet be cultivated, there may be
much we are missing out on regarding the psychrophilic life cycle.
As illustrated, evidence for the activity and replication of microorganisms at
sub-zero temperatures is now increasingly abundant. The question is not “Are
microorganisms active at sub-zero temperatures?”; the unknowns are “Is there a
low temperature limit of life?”, “What abiotic mechanisms govern microbial life
cycles at sub-zero temperatures?” and “What impact do cryoactive microbiota have
on ecosystem function and global scale biogeochemical cycling?”.
Cryoenvironments at the edge of known habitability, where microorganisms are
the only organisms present, are ideal natural laboratories to approach these
questions.
6 When the Vital Signs of Microbial Life Go Cold, Does That Mean the Pulse Is. . .
117
along with nutrients, for example, as seen in sea ice (Junge et al. 2004). Indeed,
halotolerance seems to be a phenotypic trait shared by all psychrophilic organisms
isolated to date. At sufficiently low temperatures, even highly concentrated brines
may freeze to a mere film of water adsorbed to mineral particles. This is a condition
where life is likely operating at the limits and activity is questionable. Additionally,
the nature of the salts present also plays a role in microbial survival, as differing salts
have different freezing points as well as different disordering properties which may
be disruptive to cells (Hallsworth et al. 2007; Pontefract et al. 2017). As a result of
understanding the added physiological stresses of sub-zero temperatures, the term
cryophile is increasingly being used to denote organisms that grow at sub-zero
temperatures, as opposed to psychrophiles, defined as having growth optima at
temperatures between 5
C and 15
C (Raymond-Bouchard et al. 2018; Cavicchioli
2006; Seckbach 2013).
Sub-zero growth has been observed in microorganisms with broad phylogenic
distribution and in all three domains of life. The current record for bacterial cellular
division at low temperature is À15
C by Planococcus halocryophilus OR1, a
bacterium isolated from Arctic active-layer soils (the top layer above permafrost
that thaws seasonally in the summer) (Mykytczuk et al. 2013; Raymond-Bouchard
and Whyte 2017). Other examples include Methanococcoides burtonii, an Archaeal
methanogen isolated from Ace Lake, Antarctica, and that can divide at À2.5
C
(Williams et al. 2011), and Rhodotorula glutinis FMT157, a yeast isolated from
spoiled commercial frozen peas and that can grow at À18
C (Collins and Buick
1989). This latter frozen pea isolate hints to a potentially overlooked aspect of
low-temperature microbiology—that psychrophilic microorganisms may be more
abundant and ubiquitous than expected. While most psychrophilic organisms have
been isolated from polar environments considered by humans to be relatively
“extreme”, much of the northern hemisphere that is densely populated by humans
(e.g. the cities of Toronto, or Montreal) undergoes a deep freeze regularly, encountering sub-zero temperatures for 4–6 months. It is quite probable that psychrotolerant
or possibly even psychrophilic organisms exist in the many northern environmental
niches that humans would not consider “extreme.” These examples of sub-zero
replication are known from isolated microbial cultures grown in laboratories. However as the vast majority of microorganisms cannot yet be cultivated, there may be
much we are missing out on regarding the psychrophilic life cycle.
As illustrated, evidence for the activity and replication of microorganisms at
sub-zero temperatures is now increasingly abundant. The question is not “Are
microorganisms active at sub-zero temperatures?”; the unknowns are “Is there a
low temperature limit of life?”, “What abiotic mechanisms govern microbial life
cycles at sub-zero temperatures?” and “What impact do cryoactive microbiota have
on ecosystem function and global scale biogeochemical cycling?”.
Cryoenvironments at the edge of known habitability, where microorganisms are
the only organisms present, are ideal natural laboratories to approach these
questions.
6 When the Vital Signs of Microbial Life Go Cold, Does That Mean the Pulse Is. . .
117