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AQUATIC MICROBIAL ECOLOGY
Aquat Microb Ecol
Vol. 53: 13–19, 2008
doi: 10.3354/ame01220
Printed September 2008
Published online September 18, 2008
Contribution to AME Special 1 ‘Progress and perspectives in aquatic microbial ecology’
OPEN
ACCESS
Microbial services: challenges for microbial
ecologists in a changing world
Hugh Ducklow*
The Ecosystems Center, Marine Biological Laboratory, Woods Hole, Massachusetts 02543, USA
ABSTRACT: Bacteria, archaea and other microbes have dominated most biogeochemical processes
on Earth for > 99% of the history of life, but within the past few decades anthropogenic activity has
usurped their dominance. Human activity now impacts every ecosystem on the planet, necessitating
a new socio-ecological view of ecosystem processes that incorporates human perceptions, responses,
activities and ideas into ecology. The concept of ecosystem services is an important link between
ecosystem processes and the social sphere. These include the provisioning, regulating, cultural and
supporting benefits that ecosystems provide to enhance human well-being. Many ecosystem services
are provided by microbes, initiating the concept of microbial services to society — an idea long appreciated by microbial ecologists. Experimental studies of the biodiversity–ecosystem function relationship emphasizing microbial functions are inconclusive, with increasing diversity sometimes being
observed to enhance function, while at other times the opposite relationship has been found. A specific function addressing the role of bacteria in helping or hindering carbon storage in the deep ocean
in response to iron fertilization is similarly uncertain. Bacteria respond positively to mesoscale iron
additions in many cases, but in doing so, may retard carbon storage by decomposing sinking particles. Human exploitation of microbial services to enhance planetary sustainability must be based on
focused studies of microbial processes in a human-dominated world.
KEY WORDS: Ecosystem services · Microbial services · Microbial diversity function · Sustainability ·
Iron fertilization
Resale or republication not permitted without written consent of the publisher
Earth and its component ecosystems are dominated
by 2 vastly different sets of processes. For at least 75%
of the 4 billion year history of life, bacteria and archaea
controlled elemental cycling, organic matter production and turnover and the planetary climate. In many
ways, they still do. Microbes including bacteria,
archaea, phytoplankton, protozoans and fungi still catalyze the major transformations of the elements, break
down organic matter, and produce and consume oxygen and carbon dioxide (Smil 2003). Around half the
global net primary productivity is by unicellular phytoplankton in the sea (Falkowski et al. 2000), and most
of the global respiration (terrestrial and marine) is
microbial. However, just within the past century
(0.00000001% of the history of life), many processes on
earth have become dominated by anthropogenic activities. Vitousek et al. (1997) describe the extent of
anthropogenic contributions to earth system processes.
To name but a few of the examples given by those
authors: over 60% of all marine fisheries are fully
exploited, overexploited or depleted; over 20% of all
bird species on earth have become extinct; and 50% of
all accessible surface freshwater is used in human
activity. The extent of human perturbation of the
chemical composition of the atmosphere is well
known: the CO2 concentration has increased by nearly
40% since 1750. The transformation in the nitrogen
cycle is even more striking. Human activity now
*Email: [email protected]
© Inter-Research 2008 · www.int-res.com
INTRODUCTION
14
Aquat Microb Ecol 53: 13–19, 2008
accounts for more than half of all reactive nitrogen
entering terrestrial ecosystems — an increase of over
100% in the global nitrogen cycle. Here, I suggest the
importance of recognizing the shared dominance of
the planet by the extreme ends of the evolutionary process: microbes and man. Space limits this to a cursory
treatment, with most specific examples emphasizing
bacteria. I hope the tables and references will spur
readers to further investigation.
ECOSYSTEM SERVICES
With every ecosystem on earth influenced by
humans (Palmer et al. 2004), it is necessary and
inescapable to view human beings and their activities
as integral components of ecosystems, not isolated
external drivers. Humans act on and are acted upon by
ecosystems, forming a complex network of feedback
relationships (Fig. 1). In this model of the ‘socio-ecological system’ are 3 groups of interacting components: (1)
climate, influenced by external drivers, biogeochemical processes and human activity; (2) ecosystems as
they are typically viewed, with populations, communities and biogeochemical cycles; and (3) the social system, consisting of human communities and cultures,
institutions and their actions. The climate box (Box 1) is
studied by climatologists and biogeochemists; Box 2 is
served by traditional ecology and most of Box 3 by
sociology, economics, political science, etc. New studies of socio-ecological systems (e.g. Fig. 1) seek to
unify these disciplines in a new field that includes both
traditional and human ecology as well as the social sciences and transdisciplinary fields such as adaptive
management and ecological economics (Odum 1971).
A key development in socio-ecology has been the
conceptualization and assessment of ‘ecosystem services’ (Table 1), the functions and services supplied by
‘natural’ ecosystems that benefit human society (Millennium Ecosystem Assessment 2005). The 4 main categories of ecosystem services include (1) Provisioning
services: generally durable goods with markets in local
to global economies; (2) Regulating services: ecosystem functions essential for maintaining complex
human societies on the planet; (3) Cultural services:
less tangible services that enhance social institutions
and enrich human well-being; and (4) Supporting services: this last category addresses the ecosystem functions that underlie and support the supply of the other
services. The ecosystem services concept is important
because it articulates in concrete terms the functions of
the world’s ecosystems as they benefit human society.
The concept enables the assessment of their condition
and trends in enhancement or degradation, as well as
their economic valuation, which is a necessary prerequisite for analysis of the socio-ecological system. There
have been several attempts, sometimes controversial,
to evaluate ecosystem services in direct monetary
terms (Odum 1971, Costanza et al. 1997).
MICROBIAL SERVICES
Even superficial consideration of Fig. 1 and Table 1
will suggest to microbial ecologists what we already
Table 1. Ecosystem services: 4 major types and examples
Provisioning services
• Foods (including seafood and game) and spices
• Wood and fiber (animal and vegetable fibers)
• Precursors to pharmaceutical and industrial products
• Fuel (hydropower, biomass fuels)
Regulating services
• Carbon sequestration and climate regulation
• Flood regulation
• Disease regulation
• Waste decomposition and water purification
Fig. 1. A new socio-ecological framework providing the basis
for exploring research questions about the interplay of human
society and the environment. The right-hand side represents
the domain of traditional ecological research; the left-hand
side (Box 2) represents human dimensions of environmental
change; the two are linked by the services provided by
ecosystems (Box 3 at bottom), and by disturbances such as
climate change influenced or caused by human behavior
Cultural services
• Educational
• Recreational experiences (including ecotourism)
• Aesthetic (artistic inspiration)
• Spiritual (sense of place)
Supporting services
• Soil formation
• Nutrient cycling
• Primary production
15
Ducklow: Ecosystems and microbial services
know about the place of microbes in this scheme: many
essential services and functions are carried out by
microbes (even though their role is being usurped by
humans in some cases). As noted above, microbes
carry out most of the essential biogeochemical processes, regulate climate, water quality, atmospheric
composition and perform about half the total primary
production. Microbes also contribute to other services:
domesticated microbes produce food, pharmaceuticals
and fuels. Others even contribute to cultural values by
forming natural landscape elements with aesthetic
and recreational value (e.g. clean water for recreation,
colored hotsprings).
This immediately suggests the concept of ‘microbial
services’: the services supplied to humans by different
groups of microbes (Table 2). Microbial services are
already being exploited for commercial and environmental purposes. For example, microbial supplements
are manufactured and sold as soil additives and for
environmental cleanup of pollutants, as well as other
environmental remediation and ecosystem restoration
activities. My argument here is that microbial ecologists can contribute to socio-ecology and efforts
toward achieving global sustainability by understanding the characteristics and processes of microbial
communities that enable microbial services. Here I
expand this argument by describing 2 examples. First
I review research on the relationship between microbial (mostly bacterial) biodiversity and their ecological
functions. Next I discuss the responses of bacteria and
archaea during oceanic iron fertilization, and the
(potential) role of marine bacteria in anthropogenic
CO2 sequestration.
Microbial biodiversity–ecosystem function
relationships
There is a long list of literature concerning research
on the biodiversity–ecosystem function (BEF) relationship that relates species richness and other diversity
measures of particular taxa in specific habitats to
ecosystem functions such as productivity and grazing
(e.g. Loreau et al. 2001). However, there has been little
research focusing explicitly on the BEF relationship for
the various groups of microbes. This is certainly due in
part to the difficulty of defining microbial species and
estimating their diversity (Pedros-Alio 2006). New
developments in probing community composition suggest a vast untapped wealth of bacterial and archaeal
species diversity (Sogin et al. 2006), yet the function of
the diversity reservoir is almost entirely unknown.
Does microbial diversity enhance ecosystem function?
Bell et al. (2005) examined the relationship between
community respiration and bacterial species diversity
by creating mixtures of up to 72 culturable species in
experimental microcosms over a range of species richness (1 to 72 species). They found a significant, positive
and decelerating (log-linear) relationship between
species richness and respiration rate, with apparent
synergisms among different species. The overall positive BEF relationship reflected that found in many
studies of higher taxa. However, a more comprehensive review of BEF studies of bacteria and other
members of microbial foodwebs shows that no generalization about the size and shape of the microbial
diversity–ecosystem function relationships is possible,
at least given the few studies reported to date
Table 2. The major groups of microbes and examples of services they provide
Group
Processes
Services (see Table 1)
Heterotrophic bacteria
Organic matter breakdown,
mineralization
Decomposition, nutrient recycling,
climate regulation, water purification
Heterotrophic bacteria
Extracellular polymer production
Carbon sequestration
Photoautotrophic bacteria
Photosynthesis
Primary production
Chemoautotrophic bacteria
Specific elemental transformations
(e.g. sulfate reduction, iron oxidation)
Nutrient recycling, climate regulation,
water purification
Unicellular phytoplankton
Photosynthesis
Primary production
Archaea
Specific elemental transformations
(e.g. methanogenesis, nitrification)
Nutrient cycling, atmosphere and
climate regulation
Protozoans
Consumption and mineralization
of other microbes
Decomposition, nutrient cycling,
soil formation
Fungi
Organic matter consumption
and mineralization
Decomposition, nutrient cycling,
soil formation
Fungi (mycorrhizal)
Nutrient recycling
Primary production (indirect)
Viruses
Lysis of hosts
Nutrient cycling
16
Aquat Microb Ecol 53: 13–19, 2008
(Table 3). There is no consistent relationship, with
about equal (low) numbers of positive, negative or
inconclusive responses to increased diversity.
The following generalizations can be made about
the state of this research: of the few studies overall,
most have used cultured species. Only a few studies
examined naturally occurring bacterial plus archaeal
diversity and its relationship to in situ function
(Reinthaler et al. 2006). Most studies are thus highly
artificial, which allows isolation of the BEF relationship, but neglects other factors that may affect the
relationship and masks the true diversity. Most
importantly, few ecosystem processes (functions)
have been analyzed. In many cases, the process was
selected because it was easy to measure (e.g. bacterial biomass accumulation or production). Bacterial or
community respiration is a system-level entity, but is
a general consequence of many unrelated microbial
taxa acting in concert. As such, it may be difficult to
relate to the diversity of organisms actually carrying
out the major part of the process. Examination of
specific metabolic processes carried out by specific
groups like methane oxidizers, nitrifiers or cellulose
hydrolyzers may be a more effective approach.
Microbial BEF research is a field ripe for progress.
Bacterial roles in the ocean biological pump:
the case of iron fertilization
Storage of CO2 in the deep sea is facilitated by carbon
fixation into biomass by phytoplankton, consumption by
zooplankton and gravitational sedimentation into the
deep ocean: the aggregate process termed the biological
pump (Ducklow et al. 2001). Bacteria and protozoans can
accelerate carbon sinking and storage by producing
extracellular mucins that bind particles into larger aggregates (marine snow) that sink faster, or retard sinking
and storage by decomposing the sinking materials. The
net effect probably changes according to particular sets
of conditions and is not well-understood (Azam & Malfatti 2007). In large regions of the world, ocean primary
production and export to depth are limited by micronutrient (iron) limitation (Martin et al. 1991). Several
large ecosystem manipulation studies have been performed to examine the potential for artificial iron additions (iron fertilization) to enhance CO2 storage as a
geo-engineering strategy for reducing anthropogenic
CO2 accumulation in the atmosphere (Boyd et al. 2007;
Table 4). The studies demonstrate convincingly that iron
addition stimulates photosynthesis, macronutrient
utilization and CO2 drawdown. Whether or not carbon
export responds as well is less clear (Buesseler & Boyd
2003). If iron addition does not enhance carbon export it
cannot be an effective tool for climate change mitigation.
Carbon storage via the biological pump is an ecosystem
service that potentially has a market through trading of
carbon credits. Whether the storage can be verified for
trading is still not resolved. The exact role of bacteria and
other microbes (their service) is uncertain.
The bacterial response has been studied in some, but
not all, mesoscale iron addition experiments (Table 4).
Like the BEF relationship, the results vary. The
response of bacterial community composition (species
composition and richness) is not conclusive, but only
very few studies have examined this property. In most
Table 3. Experiments and observations relating microbial diversity and ecosystem function. Diversity is represented as the
number of added species. Natural: naturally occurring species diversity in different water samples
Habitat
Freshwater
Freshwater
Freshwater
Soil
Soil
Soil
Freshwater
Freshwater
Review
Freshwater + litter
Tree H2O
Freshwater
Freshwater
Marine
Marine
Freshwater
Freshwater
Freshwater
Diversity
31
3
High vs. Low
High vs. Low
31
High vs. Low
8
6
—
8
72
4
4
Natural
Natural
4
4
4
Variable
Relationship
Respiration (CO2)
Biomass increase
Productivity
Respiration (CO2)
Abundance increase
Respiration (CO2)
Biomass increase
Biomass increase
Respiration (CO2)
Cellulose decomposition
Respiration (CO2)
Biomass increase
Biomass increase
Production increase
Respiration increase
Decomposition
Trophic transfer
Biovolume increase
+
+
0
+
+
0
0
–
+
+
+
+
+
–
–
0
0
+
Source
McGrady-Steed et al. (1997)
Naeem & Li (1997)
Petchey et al. (1999)
Griffiths et al. (2000)
McGrady-Steed & Morin (2000)
Griffiths et al. (2001)
Petchey et al. (2002)
Gonzalez & Descamps-Julien (2004)
Morin & McGrady-Steed (2004)
Wohl et al. (2004)
Bell et al. (2005)
Steiner et al. (2005)
Steiner et al. (2006)
Reinthaler et al. (2005)
Reinthaler et al. (2005)
Jiang (2007)
Jiang (2007)
Jiang (2007)
17
Ducklow: Ecosystems and microbial services
Table 4. Responses of bacterioplankton assemblages to mesoscale iron fertilization. +: positive response; 0: no response;
—: not tested; na: not available
Study
Region/Year
Temp. (°C)
Abund/Prod?
Community shift?
IronEx1
IronEx2
SOIREE
EisenEx
SEEDS-1
SOFEX
Equatorial Pacific/1993
Equatorial Pacific/1995
Southern Ocean/1999
Southern Ocean/2000
North Pacific/2002
Southern Ocean/2002
23
25
2
4
11
–1
—
+
+
+
0
+
—
—
—
0
—
+
SERIES
North Pacific/2002
13
+
+
EIFEX
SEEDS-2
SAGE
Fee-P
CROZEX
Southern Ocean/2004
North Pacific/2004
Southern Ocean/2004
Subtropical Atlantic/2004
Southern Ocean/2004-05
5
10
12
21
2
na
na
na
0
+
na
na
na
na
+
studies, bacterial growth is stimulated following the
phytoplankton response, suggesting that bacteria may
be carbon- rather than iron-limited (Church et al.
2000). Boyd et al. (2004) calculated that most of the
organic matter produced in response to iron addition in
the northeast Pacific was consumed by bacteria. If the
bacteria are stimulated to decompose organic matter
that is produced in response to iron stimulation, their
net effect will be to lower the carbon storage efficiency.
The larger issues surrounding the iron fertilization
question are too complicated to review in any detail
here. However, one further effect is noteworthy. If iron
fertilization were effective in stimulating the biological
pump, and if it were employed as a long-term, largescale strategy (this is highly uncertain; see Sarmiento &
Orr 1991), the additional input of organic matter would
be consumed by heterotrophic microbes, possibly rendering the deep sea hypoxic or anoxic. Fuhrman &
Capone (1991) speculated that prolonged iron fertilization could result in large releases of N2O and methane,
2 powerful greenhouse gases. The net effect would be
to enhance, not ameliorate, the anthropogenic greenhouse effect. The complex effects of iron fertilization
have not borne out the initial expectations of a greenhouse panacea (Chisholm et al. 2001). As those authors
stated (p. 310): “The proponents’ claim that fertilization for carbon sequestration would be environmentally benign is inconsistent with almost everything
we know about aquatic ecosystems.”
When viewed in the context of integrated socioecological systems, including human actions and
responses such as iron fertilization, the situation originally presented in Fig. 1 is much more complicated
(Fig. 2). Iron fertilization provides one example of the
interplay of microbial processes and human actions.
Source
Martin et al. (1994)
Cochlan (2001)
Hall & Safi (2001)
Arrieta et al. (2004)
Suzuki et al. (2005)
Oliver et al. (2004),
J.L. Oliver et al.
(unpubl. data)
Boyd et al. (2004),
Hale et al. (2006),
Agawin et al. (2006)
na
na
na
Rees et al. (2007)
Zubkov et al. (2007)
Microbes and humans together influence climate
change via the ecosystem service of carbon storage,
but unintended consequences like N2O production
may add other feedbacks to this system. Thus, iron
fertilization provides a useful case study of the complex interrelationships and feedback loops that potentially exist among climate change, microbial services and social concerns, perceptions and actions,
involving microbial ecologists and the rest of society.
The brevity of this article prevents a fuller examination
of microbe–human–ecosystem–climate interactions
and feedbacks; an enormous topic. I hope it will stimulate new research — or at least second thoughts by
interested students.
Fig. 2. The same framework as in Fig. 1, specifically showing
the relationships in the socio-ecological sphere for purposeful
iron fertilization of the ocean ecosystem to mitigate anthropogenic CO2 accumulation in the atmosphere. Note in both
figures that there is no specified starting point for the network
of feedback loops in the system
18
Aquat Microb Ecol 53: 13–19, 2008
Acknowledgements. The work for this manuscript was supported in part by NSF OPP 0217282. I thank the organizers of
SAME10 for the invitation to present these ideas and David
Kirchman for helpful discussions.
➤
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19
Proofs received from author(s): July 7, 2008

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