Temperature controls on aquatic bacterial production
and community dynamics in arctic lakes and streams
Heather E. Adams,
1
* Byron C. Crump
2
and
George W. Kling
1
1
University of Michigan, Department of Ecology and
Evolutionary Biology, Ann Arbor, MI, USA.
2
University of Maryland Center for Environmental
Science, Horn Point Laboratory, Cambridge, MD, USA.
Summary
The impact of temperature on bacterial activity and
community composition was investigated in arctic
lakes and streams in northern Alaska. Aquatic bacte-
rial communities incubated at different temperatures
had different rates of production, as measured by
14
C-leucine uptake, indicating that populations within
the communities had different temperature optima.
Samples from Toolik Lake inlet and outlet were col-
lected at water temperatures of 14.2°C and 15.9°C,
respectively, and subsamples incubated at tempera-
tures ranging from 6°C to 20°C. After 5 days, produc-
tivity rates varied from 0.5 to ~13.7 mgCl
-1
day
-1
and
two distinct activity optima appeared at 12°C and
20°C. At these optima, activity was 2- to 11-fold higher
than at other incubation temperatures. The presence
of two temperature optima indicates psychrophilic
and psychrotolerant bacteria dominate under differ-
ent conditions. Community fingerprinting via denatur-
ant gradient gel electrophoresis (DGGE) of 16S rRNA
genes showed strong shifts in the composition of
communities driven more by temperature than by dif-
ferences in dissolved organic matter source; e.g. four
and seven unique operational taxonomic units (OTUs)
were found only at 2°C and 25°C, respectively, and not
found at other incubation temperatures after 5 days.
The impact of temperature on bacteria is complex,
influencing both bacterial productivity and commu-
nity composition. Path analysis of measurements of
24 streams and lakes sampled across a catchment 12
times in 4 years indicates variable timing and strength
of correlation between temperature and bacterial pro-
duction, possibly due to bacterial community differ-
ences between sites. As indicated by both field and
laboratory experiments, shifts in dominant commu-
nity members can occur on ecologically relevant time
scales (days), and have important implications for
understanding the relationship of bacterial diversity
and function.
Introduction
Bacteria are important organisms in ecosystems, perform-
ing the critical tasks of decomposing organic matter,
regenerating nutrients and forming the base of microbial
food webs. The rates of these critical tasks can be modi-
fied by temperature, and understanding the bacterial
response to temperature is necessary for understanding
ecosystem function. For example, at higher temperatures,
metabolic rates increase considerably and bacteria are
able to break down organic substrates more rapidly
(Pomeroy and Wiebe, 2001) and increase secondary pro-
duction (Kirchman and Rich, 1997). Here we examine the
links between temperature and ecosystem function as
measured by aquatic bacterial production both directly
and indirectly through alteration of bacterial community
composition.
The metabolic activity of aquatic bacteria is directly
limited by temperature in many systems. A strong relation-
ship between bacterial-specific growth rate and tempera-
ture was found in a metadata analysis of 57 studies in
freshwater, coastal and marine habitats (White et al.,
1991), and temperature limitation has been found in estu-
aries (Shiah and Ducklow, 1994; Almeida et al., 2001;
2007), sea grass beds (Danovaro and Fabiano, 1995),
rivers (Freese et al., 2006), coastal systems (Sherr et al.,
2001), marine systems (Longnecker et al., 2006), and
lakes of various nutrient regimes (Sommaruga and
Conde, 1997; Simon and Wunsch, 1998; Friedrich et al.,
1999; Gurung and Urabe, 1999; Ram et al., 2005; Vrede,
2005) including high arctic lakes (Panzenbock et al.,
2000). A few studies found that temperature is not limiting
to bacteria; in these studies only small increases in tem-
perature were tested (Ducklow et al., 1999), or it was
found that carbon quality was more important (Mcknight
et al., 1993).
Temperature can also interact with carbon availability or
substrate affinity to control bacterial activity. At colder
temperatures, bacteria begin to lose substrate affinity,
leading to carbon limitation despite available sources in
Received 14 July, 2009; accepted 25 December, 2009. *For corre-
spondence. E-mail hea@umich.edu; Tel. (+1) 734 647 0898; Fax
(+1) 734 763 0544.
Environmental Microbiology (2010) 12(5), 1319–1333 doi:10.1111/j.1462-2920.2010.02176.x
© 2010 Society for Applied Microbiology and Blackwell Publishing Ltd