Biogeochemical Consequences of Rapid Microbial Turnover and Seasonal Succession in Soil

Author(s): S. K. Schmidt, E. K. Costello, D. R. Nemergut, C. C. Cleveland, S. C. Reed, M. N.

Weintraub, A. F. Meyer and A. M. Martin
Source: Ecology, Vol. 88, No. 6 (Jun., 2007), pp. 1379-1385
Published by: Wiley
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Ecology, 88(6), 2007, pp. 1379-1385
? 2007 by the Ecological Society of America

BIOGEOCHEMICAL CONSEQUENCES OF RAPID MICROBIAL TURNOVER

AND SEASONAL SUCCESSION IN SOIL
S. K. Schmidt,1 4 E. K. Costello,1 D. R. Nemergut,2'3 C. C. Cleveland,3 S. C. Reed,1'3 M. N. Weintraub,1
A. F. Meyer,1 and A. M. Martin1
x Department of Ecology and Evolutionary Biology, University of Colorado, Boulder, Colorado 80309 USA
Environmental Studies Program, University of Colorado, Boulder, Colorado 80309 USA
3Institute of Arctic and Alpine Research, University of Colorado, Boulder, Colorado 80309 USA

Abstract. Soil microbial communities have the metabolic and genetic capability to adapt
to changing environmental conditions on very short time scales. In this paper we combine
biogeochemical and molecular approaches to reveal this potential, showing that microbial
biomass can turn over on time scales of days to months in soil, resulting in a succession of
microbial communities over the course of a year. This new understanding of the year-round
turnover and succession of microbial communities allows us for the first time to propose a
temporally explicit N cycle that provides mechanistic hypotheses to explain both the loss and
retention of dissolved organic N (DON) and inorganic N (DIN) throughout the year in
terrestrial ecosystems. In addition, our results strongly support the hypothesis that turnover of
the microbial community is the largest source of DON and DIN for plant uptake during the
plant growing season. While this model of microbial biogeochemistry is derived from observed
dynamics in the alpine, we present several examples from other ecosystems to indicate that the
general ideas of biogeochemical fluxes being linked to turnover and succession of microbial
communities are applicable to a wide range of terrestrial ecosystems.
Key words: microbial community composition; nitrogen cycle; seasonal dynamics; succession; under
snow growth.

Introduction along environmental gradients within minutes in re

Microorganisms experience time and space on scales sponse to pulses of limiting resources (e.g., Garcia
that are currently under-appreciated in the fields of Pichel and Pringault 2001, Fenchel 2002).
ecology and evolutionary biology. A typical bacterium is The profound implications of scale are especially
almost 1 X 107 times smaller and can have a generation important in the soil microenvironment. Arguably, soil
time 1 X 107 times shorter than an animal such as an comprises the most spatially and temporally heteroge
elephant. To put this in perspective, an elephant is about neous environment on Earth; a combination of complex
1 X 107 times smaller than the planet Earth (Koch 1976). physical structure, geochemistry, and dramatic seasonal
Therefore, in many respects bacteria (as well as archaea fluctuations in temperature, moisture and nutrient
and the slightly larger microbial eukaryotes), live on a availability are all experienced by soil microbes at
scale that is closer to the molecular world than it is to the micro-scales. It is therefore no surprise that soils have
world of macroorganisms like elephants and plants been shown to have higher diversity and biomass of
(Purcell 1977). In the microbial world, time is speeded microbes compared with other environments (Torsvik et
up relative to our experience. A combination of short al. 2002). Indeed, the total number of microbial species
generation times, rapid evolutionary potential, and large in soil remains unknown (Schloss and Handelsman
surface-to-volume ratios give soil microbes distinct 2004). Yet, the nature of soil itself has restricted our
advantages over plants and animals in terms of how view of microbial ecology in terrestrial environments.
quickly they can process resources and adapt to change The small spatial scale of soil microbial community
in natural environments. Therefore, microorganisms dynamics, soil's complex matrix of minerals and organic
matter have made it difficult to extract microbes or their
have the ability to perceive and respond to environmen
tal changes on a much faster time scale than plants and cellular constituents from soil or to use cell sorting and
animals. For example, microbes can sense changing DNA probing techniques that have led to major recent
gradients of limiting resources in seconds to minutes, advances in marine microbial ecology (e.g., Boetius et al.
allowing them to come out of dormancy and even move 2000, K?nneke et al. 2005). In addition, and perhaps
most importantly, most soil microbes have yet to be
cultured outside of the soil environment (Rapp? and
Manuscript received 1 February 2006; revised 28 June 2006;
accepted 17 July 2006. Corresponding Editor: R. B. Jackson.
Giovannoni 2003, Janssen 2006). However, with the
For reprints of this Special Feature, see footnote 1, p. 1343. advent of cultivation-independent assessments of micro
4 E-mail: [email protected] bial diversity, high-throughput DNA sequencing tech
1379

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 1380 S. K. SCHMIDT ET AL. Ecology, Vol. 88, No. 6

nologies and advances in isotopic approaches, we are small fraction of the microbial N released in the
beginning to glimpse the vast diversity and adaptability rhizosphere this is an important source of N for plants
of microbes in soil, both from spatial and temporal in natural ecosystems. In alpine soils, plants only have to
perspectives. capture about 5% of the N released by turnover of
Here, we explore how recent advances in molecular microbial N to meet their N demands for growth (Fisk
and isotope techniques are allowing us to begin to et al. 1998). The ecosystem-level consequences of the
understand the dynamics of microbial communities and intermeshing of rapid microbial N turnover and the
how those dynamics link to major biogeochemical slower cycling of plant N are discussed in more detail
processes in soil. In particular we focus on recent work below (See A Temporally Explicit N Cycle).
in the tundra and forests of Colorado that links turnover
and seasonal succession of microbial communities with Seasonal succession in microbial communities
the timing and magnitude of nitrogen (N) and carbon That some microbial communities can undergo
1(C) flow through those systems. successional changes on time scales of less than one
Microbial Turnover and Succession in Soil year has been hypothesized since the 1950s (see
references in Thormann et al. 2003). Most data
High rates of microbial turnover in soil supporting this idea have come from studies of enzyme
Initial evidence of high rates of microbial turnover in activity (reviewed by Sinsabaugh et al. 2002, Sinsabaugh
alpine soils came from 15N-dilution approaches previ 2005) and fungal community structure (reviewed by
ously used to demonstrate high rates of microbial Thormann et al. 2003) during the decomposition of
organic matter in soil. In addition, work examining
biomass N (MBN) turnover in a diversity of forest soils
(e.g., Stark and Hart 1997). In soils of three widespread microbial succession in recently deglaciated soils sup
alpine plant communities of the Rocky Mountains, Fisk ports the idea that microbial communities can show
et al. (1998) found that microbial immobilization of N successional changes on much shorter time scales than
exceeded gross rates of N mineralization. The underly succession of plant communities (see Nemergut et al., in
ing reason for the rapid immobilization of mineralized N press, and references therein).
was that the microbial pool was turning over much Our initial studies of seasonal succession in alpine
faster than was previously thought creating a sustained soils grew out of the turnover studies discussed above
N sink. Fisk et al. (1998) estimated a mean residence and indicated that many microbial functional groups
time of 0.05 years for N in the microbial biomass, which show dramatic seasonal changes (Lipson et al. 2002). As
translates to a turnover time of 18 days. This estimate an example, Fig. 1 shows the seasonal variation of
agreed with the work of Lipson et al. (2001) who used salicylate-mineralizing microbes in alpine meadow soils.
different methods, data sets, and field sites than Fisk et In agreement with other independent measures of
al. (1998) and found that amino acid N turns over every biomass and enzymatic activity (Lipson et al. 1999),
13 days through the microbial biomass. While the microbial biomass in this system peaked under late
estimates of Fisk et al. (1998) and Lipson et al. (2001) winter snow packs. In addition, soil cellulase activity
are towards the low end of the range of microbial N peaks in late winter (Lipson et al. 2002), explaining why
turnover times in soils (e.g., compare Holmes and Zak a high percentage of plant litter decomposition takes
1999), faster turnover times have been reported for more place in the winter in many seasonally snow-covered
productive systems; for example, Perakis and Hedin ecosystems (Taylor and Jones 1990, Hobbie and Chapin,
(2001) estimated a microbial N turnover time of 9 days 1996, Schmidt and Lipson 2004). The under-snow peak
in an unpolluted forested ecosystem in Chile. Other in microbial biomass and cellulase activity was followed
studies (e.g., Davidson et al. 1992, Stottlemeyer and by a precipitous biomass decline during snowmelt that
Toczydlowski 1999, Grenon et al. 2005) also indicate resulted in a large release of available DON and DIN.
that high rates of gross N mineralization and immobi This N is then taken up by plants and later successional
lization are common in diverse ecosystems, suggesting microbes (Mullen et al. 1998, Jaeger et al. 1999) or is lost
that the turnover of microbial N is also rapid. to the system via leaching (Brooks et al. 1998). The
Recent studies point to the rhizosphere as the site of release of available N during snowmelt coincides with
the most rapid N mineralization and microbial turnover the highest year-round levels of protease activity (Lipson
in soil (Hamilton and Frank 2001, Ostle et al. 2003, et al. 1999) indicating that the snow-melt microbial
Staddon et al. 2003, Butler et al. 2004, Rangle-Castro et community is largely fueled by protein released from the
al. 2005). The rhizosphere is an environment where root crash of the winter microbial community. Microbial
exudates stimulate microbes that have the potential to biomass has a much higher protein concentration than
rapidly initiate growth following a DOM pulse. These plant litter, for example bacteria are over 50% protein by
growth spurts lead to increased pr?dation by protists weight (Neidhardt et al. 1990). Finally, the microbial
and larger soil eukaryotes (reviewed by Clarholm 1985, community that develops in the summer is fueled mostly
Moore et al. 2003) resulting in increased microbial by rhizodeposition (Lipson et al. 2002). In summary,
turnover and leakage of DON and DIN back into the substrate availability and enzyme activity data indicate
rhizosphere environment. Even if plants only take up a that there is a yearly succession of dominant substrates

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June 2007 NEW DIRECTIONS IN MICROBIAL ECOLOGY 1381

Fig. 1. Two demonstrations of the extreme seasonality of microbial communities in soil. (A) Seasonal changes (mean ? SE) in
soil microbes that mineralize salicylic acid to C02 at 3?C (psychrophiles) and 22?C (mesophiles). Soil temperatures (5 cm depth)
ranged from -0.5?C (27 April) to a summer average of 11?C (30 June, 29 July, and 7 September) and 6?C in the fall (5 October).
Soils were frozen too solid (less than ?5?C) to measure soil temperature on the first sampling date (11 February). The arrows on
either side of "snow cover" indicate the temporal extent of snow cover during the study. Data for mesophilic microbial biomass for
June, July, and August were previously published (Schmidt et al. 2000). (B) Saprotrophic "snow mold" forming a dense hyphal mat
on litter of a spruce-pine forest that shows high levels of under-snow C02 flux (Monson et al. 2006). This snow mold disappears
within days of the soils becoming snow-free.

for microbial growth progressing from carbon polymers/ in our study (Fig. 2B; Lipson and Schmidt 2004), Tl
phenolics (winter) to proteins (snowmelt) to rhizodepo indicating that sub-groups of the Acidobacteria may be q
sition (summer). involved in many other soil processes besides protein >
degradation. Moreover, their sustained presence in the r
Observation of the seasonal succession of functional
groups prompted phylogenetic studies of seasonal soil may indicate that, in general, they are more K- "H
fluctuations of the microbial community in tundra soils. selected than some other groups of bacteria (see Fierer et >
From a broad phylogenetic perspective, fungi dominate al. 2007). It should be noted, however, that much more C
the under-snow biomass and bacteria are more active in detailed molecular work is needed to definitively link ^
the summer (Lipson et al. 2002, Schadt et al. 2003). phylogeny and function in soil ecosystems, especially for
These observations are in agreement with studies from largely uncultured groups such as the Acidobacteria and
other systems that also show that fungi dominate Verrucomicrobia.
microbial biomass in the winter (Myers et al. 2001, Microbial eukaryotes also show significant seasonal
Bardgett et al. 2005). At a finer taxonomic scale, the succession, but in all seasons fungi dominate alpine soils
phylogenetic makeup of both the bacterial and fungal (Schadt et al. 2003). Within the fungi there are also large
communities change dramatically from season to season seasonal changes in the major groups of the fungi
(Schadt et al. 2003, Lipson and Schmidt 2004). In fact, (Ascomycetes, Basidiomycetes, and Zygomycetes), but
the soil bacterial community shows more seasonal than the most dramatic changes occur within previously
spatial variation in alpine tundra soils (Lipson and unknown subphylum level clades of Ascomycetes (Fig.
Schmidt 2004). This seasonal succession of bacteria (Fig. 2A). The functional roles of these new groups of fungi
2B) also provides mechanistic insights into the season remain to be uncovered but it is apparent in Fig. 2A that
ally of biogeochemical fluxes from these soils. For Group II shows less seasonal fluctuation than Group I
example, the winter-dominant CFB group contains and therefore may be more A^-selected than Group I.
many known degraders of cellulose and lignin and their Conversely Group I is probably more r-selected and its
presence under the snow agrees with independent rapid rise during the growing season may indicate that it
observations of high de-polymerase activity and litter is a rhizosphere inhabitant. Indeed, recent soil meta
decomposition under the snow. Furthermore, although genomic studies have uncovered Group I during the
much less is known about the Acidobacteria and growing season in forest soils from Canada to Costa
Rica and have confirmed that the closest known
Verrucomicrobia, the successional progression of sub
strates discussed above indicates that some of these relatives to this group are relatively fast growing
organisms may be associated with snowmelt proteolysis ascomycetous yeasts (T. M. McLenon, personal commu
(Acidobacteria) and rhizosphere dynamics (Verrucumi nication).
crobia). In addition, the Acidobacteria showed the least Evidence of seasonal succession of microbial commu
seasonal variation among the major bacterial divisions nities in soils is also accumulating from ecosystems other

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 1382 S. K. SCHMIDT ET AL. Ecology, Vol. 88, No. 6
100 n photosynthesis per year is respired by under-snow
microbial activity (Monson et al. 2006). Like tundra
soils, these soils exhibit significant changes in the
80 H bacterial (Monson et al. 2006) and fungal (Fig. IB)
communities from winter to summer. Unlike tundra,
however, under-snow microbial activity in these forests
is fueled by rhizodeposition in addition to litter
60 H
decomposition (M. Weintraub, unpublished data).

Succession in the rhizosphere

0
?CO 40H Evidence of succession of microbial communities has
D
c
also recently come from detailed molecular studies of
rhizosphere communities (e.g., Smalla et al. 2001,
CO
0 20 Gomes et al. 2003) and long-term studies of root
> colonizing fungi in alpine ecosystems. The rhizosphere is
Group I
CD a very dynamic environment that receives large inputs of
- Group II
C substrates from plants (e.g., Norton et al. 1990). These
E
3
Under-snow Snowmelt Summer C inputs fuel the rapid growth and subsequent turnover
E
x of r-selected microbes leading to increased N availability
CO
E 100' to plants (Clarholm 1985, Moore et al. 2003), but they
Q. can also sustain longer-term, more ^-selected rhizo
O sphere inhabitants such as mutualistic bacteria (Hirsch
et al. 2003) and fungi (Smith and Read 1997). The most
80' widespread, and best studied, examples of these fungi
Id are the arbuscular mycorrhizal (AM) fungi. AM fungi
rr c
=> 0 allow plants to increase surface area for nutrient uptake,
0 60 H access nutrients beyond the rhizosphere, and directly
Id CL obtain organic forms of N in soil (Smith and Read 1997,
Hodge et al. 2001). In addition, plants can regulate their
< involvement with AM fungi in response to their
40
O immediate nutrient requirements (reviewed by Koide
Ld
CL and Schreiner 1992) and recent demonstration of
(f) unexpectedly fast (5-6 day) turnover time of C
20 associated with AM fungi (Staddon et al. 2003) indicates
a high potential for successional change of these fungi
on plant roots.
Studies of mycorrhizal fungi in alpine soils have
Under-snow Snowmelt Summer provided some of the only field-based evidence that plants
can use a succession of different fungal partners to access
Fig. 2. Seasonal succession of some major microbial groups
in alpine dry meadows. (A) Novel ascomycete fungal groups different soil nutrients over the course of a growing
and (B) the dominant bacterial divisions in alpine soil. Relative season. We observed succession of fungal partners in the
abundances of groups were derived from phylogenetic analyses roots of Ranunculus adoneus (Fig. 3) and found that
of season-specific (A) fungal (Schadt et al. 2003) and (B) phosphorus uptake by this plant coincided with the
bacterial (Lipson and Schmidt 2004) rRNA libraries and are
expressed as percentage of maximal observed seasonal abun
transitory (less than two weeks) abundance of AM
arbuscules in new roots of this plant in the field (Mullen
dance to emphasize temporal fluctuations for each group. Solid
lines represent dynamics for changes in abundance of each and Schmidt 1993). In contrast, all N uptake in R. adoneus
group in replicate samples collected under snow, at snow melt, occurred during and just after snowmelt when the over
and in the summer. Dashed lines represent potential trajectories
wintering roots were heavily infected with a novel
through fall (unsampled period). Abbreviations are: ?cidos,
Acidobacteria; Verrucos, Verrucomicrobia; CFB, Cytophaga endophytic fungus (Mullen et al. 1998). This endophyte
Flexibacter Bacteroides. has since been identified (Schadt et al. 2001) and shown to
have high affinity uptake systems for multiple forms of
organic (proteins and amino acids) and inorganic N
than the alpine. For example, recent studies of (nitrate and ammonium) at temperatures that occur in the
coniferous forests of the Rocky Mountains are revealing field during snowmelt (0-3?C; S. K. Schmidt, unpublished
significant seasonal succession of microbial communities data). Thus, it is likely that R. adoneus uses these fungal
that largely explain seasonal patterns of soil respiration endophytes to access the snowmelt pulse of N in alpine
(Monson et al. 2006). These soils are extremely active in soils. Some other common alpine plants (e.g., Acomastylis
the winter and over 50% of the carbon assimilated via rossii) are also able to take up the early season pulse of N

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June 2007 NEW DIRECTIONS IN MICROBIAL ECOLOGY 1383

Q. 150
we summarize this understanding as a temporally
O
<-N uptake-> <-P uptakes explicit model of the N cycle in alpine tundra. While
? this model is representative of observed dynamics in the
CO alpine, we believe that the general ideas of microbial
0
turnover during the plant growing season and large
fluxes of N during seasonal transitions of microbial
o loo DSE
? communities are generally applicable even though the
0 timing and magnitude of these events will vary from
system to system.
E
Recent models of N cycling have emphasized plant
E uptake of amino acids and microbial de-polymerization
x
C0
E 50 of plant litter as important and underappreciated
aspects of N cycling in soil (Neff et al. 2003, Schimel
0
O)
and Bennett 2004, Chapman et al. 2006). What Fig. 4
?
c
adds to these models is an understanding of the different
0 time scales on which microbial and plant nutrient
2 cycling occur. With regards to de-polymerization, the
& O1? discovery of wintertime peaks in fungal biomass, and de
June July August September October polymerizing bacteria (the CFB group) combined with
Fig. 3. Seasonal succession of fungal endophytes within the high rates of de-polymerase enzyme activity under the
roots of field-collected snow buttercup plants (Ranunculus snow, indicate that there is a temporal separation of the
adoneus). The three types of fungi are dark septate endophytes major period of de-polymerization from the period of
(DSE), arbuscules of coarse AM fungi (arbuscules), and hyphae
plant N uptake. In addition, the snowmelt peak of
of a fine AM endophyte (FE). DSE were quantified in
overwintering roots and correspond with the period of N uptake microbial death and proteolysis provides the largest
by this plant. Arbuscules and the FE appeared in new roots just year-round pulse of DON and DIN, some of which can /a
prior to and during net phosphorus uptake by these plants in the be taken up by specific plants (e.g., R. adoneus and A. tj
field. Angle brackets at the top of the figure indicate the
rossii). But for many alpine plants (e.g., Deschampsia q
measured period during which most (>90%) of the uptake
occurred for each element. Data are redrawn from Mullen and caespitosa, Kobresia myosuroides) most N uptake occurs >
Schmidt (1993) and Mullen et al. (1998). Error bars indicate later in the summer (Jaeger et al. 1999) and is driven by r
?SE. the rapid turnover of the microbial N cycle in the "H
rhizosphere (Fig. 4). >
(Jaeger et al. 1999), but the role of fungal succession has Year-round seasonal succession of microbial groups C
not been studied in these species. and rapid turnover of microbial biomass also offer a ?B
mechanistic hypothesis for how available N (DON and
A Temporally Explicit N Cycle DIN) is both retained and lost from ecosystems. With
Results from temporal studies of N fluxes, microbial each turnover event or successional cycle, most N from
succession and turnover and timing of plant N uptake the previous cycle is retaken up by microbes (Fisk et al.
discussed above have provided the first year-round 1998, Lipson et al. 2001) while a smaller proportion is
picture of N cycling in any natural ecosystem. In Fig. 4, lost to leaching or plant uptake (Fig. 4). There should

Fall/winter N cycle Summer N cycle

Plant N
' Winter microbial N cycle;
high de-polymerase activity
Summer microbial N cycle
(turns over ~1 Ox)
>DN uptake
^and biomass buildup
h (turns over 1-2x)

Fig. 4. A conceptual model of the succession of N cycles and losses from seasonally snow-covered ecosystems based on year
round studies of alpine meadows. From left to right, the fall/winter cycle is a time of microbial buildup (low turnover), high de
polymerase activity, and immobilization of N into microbial cells. At snow melt-out, the cold-adapted (psychrophilic) microbial
biomass crashes, resulting in release of dissolved N (DN). Some of this N is retained by growth of the snowmelt microbial
community and overwintering endophytic fungi or is lost to leaching. N in the summer microbial community turns over
approximately 10 times (N turnover time of 13-18 days) and each turn of the microbial cycle releases DON and DIN. Most of this
N is rapidly retaken up by the microbial biomass, but some may be taken up by plants and/or lost to leaching. The magnitude of N
losses during the summer should be directly related to the rapidity of microbial turnover and relative plant demand for N.

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 1384 S. K. SCHMIDT ET AL. Ecology, Vol. 88, No. 6

therefore be a positive relationship between microbial and the use of data. This work was supported by grants from
turnover rates and N losses but more research is needed the National Science Foundation of the USA (MCB0084223,
to test this hypothesis in other ecosystems. Better MCB0455606, DEB0455606, and IBN-0212267). The Niwot
Ridge LTER program and the Mountain Research Station at
understood is the relationship between major seasonal the University of Colorado provided logistical support for the
transitions in microbial communities and N loss and field portions of this work.
retention by ecosystems. In the alpine, the major Literature Cited
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