Biogeochemistry of marine dissolved organic matter

698 Pages·2014·65.15 MB·English

by  Dennis A Hansell, Craig A Carlson

BIOGEOCHEMISTRY OF MARINE DISSOLVED
ORGANIC MATTER
SECOND EDITION
BIOGEOCHEMISTRY
OF MARINE
DISSOLVED
ORGANIC MATTER
SECOND EDITION
Edited by
Dennis A. HAnsell
Rosenstiel School of Marine and Atmospheric Science
University of Miami
Miami, Florida
and
CrAig A. CArlson
Department of Ecology Evolution And Marine Biology
University of California
Santa Barbara, California
AMSTERDAM BOSTON HEIDELBERG LONDON NEW YORK OXFORD
PARIS SAN DIEGO SAN FRANCISCO SYDNEY TOKYO
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Dedication
For the support and balance that only family can and our children Allison and Rachel, and Matthew,
provide we dedicate this book to our parents Paul Hayden and Sydney. The foundation they have
and Rose Marie Hansell and David and Paula provided us is, through this book, extended to
Carlson, our beloved spouses Paula and Alison coming generations of marine scientists.
v
List of Contributors
Rainer M.W. Amon Department of Marine Sciences David M. Karl Daniel K. Inouye Center for Microbial
and Oceanography, Texas A&M University at Oceanography: Research and Education, Depart-
Galveston, Galveston, Texas, USA ment of Oceanography, School of Ocean and Earth
Thomas R. Anderson National Oceanography Science and Technology, University of Hawaii,
Centre Southampton, Southampton, UK Honolulu, Hawaii, USA
Leif G. Anderson Department of Chemistry and David J. Kieber College of Environmental Science
Molecular Biology, University of Gothenburg, and Forestry, Department of Chemistry, State Uni-
Gothenburg, Sweden versity of New York, Syracuse, New York, USA
Sandra Arndt School of Geographical Sciences, Tomoko Komada Romberg Tiburon Center, San
University of Bristol, Bristol, UK Francisco State University, Tiburon, California, USA
Steven R. Beaupré Geology and Geophysics, Woods Caroline Leck Department of Meteorology, Univer-
Hole Oceanographic Institution, Woods Hole, sity of Stockholm, Stockholm, Sweden
Massachusetts, USA Kenneth Mopper Department of Chemistry and
Biochemistry, Old Dominion University, Norfolk,
Karin M. Björkman Daniel K. Inouye Center for
Virginia, USA
Microbial Oceanography: Research and Education,
Department of Oceanography, School of Ocean and Norman B. Nelson Earth Research Institute, Uni-
Earth Science and Technology, University of versity of California Santa Barbara, California, USA
Hawaii, Honolulu, Hawaii, USA Mónica V. Orellana Polar Science Center, Univer-
Deborah A. Bronk Virginia Institute of Marine sity of Washington/Institute for Systems Biology,
Science, College of William & Mary, Virginia, USA Seattle, Washington, USA
David J. Burdige Department of Ocean, Earth and Peter A. Raymond Yale School of Forestry and Envi-
Atmospheric Sciences, Old Dominion University, ronmental Studies, New Haven, Connecticut, USA
Norofk, Virginia, USA Daniel J. Repeta Department of Marine Chemistry
Craig A. Carlson Department of Ecology, Evolution and Geochemistry, Woods Hole Oceanographic
and Marine Biology, University of California, Santa Institution, Woods Hole, Massachusetts, USA
Barbara, California, USA Andy Ridgwell School of Geographical Sciences,
James R. Christian Fisheries and Oceans Canada, University of Bristol, Bristol, UK
Canadian Centre for Climate Modelling and Anal- Chiara Santinelli Istituto di Biofsica, Pisa, Italy
ysis, Victoria, British Columbia, Canada Rachel E. Sipler Virginia Institute of Marine Science,
Thorsten Dittmar Research Group for Marine Geo- College of William & Mary, Virginia, USA
chemistry (ICBM-MPI Bridging Group), Institute Robert G.M. Spencer Department of Earth, Ocean
for Chemistry and Biology of the Marine Environ- and Atmospheric Science, Florida State University,
ment (ICBM), University of Oldenburg, Olden- Tallahassee, Florida, USA
burg, Germany Colin A. Stedmon National Institute of Aquatic
Kevin J. Flynn Centre for Sustainable Aquatic Resources, Technical University of Denmark,
Research, Swansea University, Swansea, UK Charlottenlund, Denmark
Dennis A. Hansell Rosenstiel School of Marine and Aron Stubbins Skidaway Institute of Oceanogra-
Atmospheric Science, University of Miami, Miami, phy, Department of Marine Sciences, University of
Florida, USA Georgia, Savannah, Georgia, USA
xi
Foreword
As one of Earth’s largest exchangeable carbon refractory DOM pool. A challenge is to under-
reservoirs, similar in scale to atmospheric CO2, stand the biological and physicochemical forces
the biogeochemical behavior of marine dis- that mediate and regulate the biogeochemical
solved organic matter (DOM) has major signif- behavior of various DOM components.
icance for the carbon cycle, climate, and global Most oceanic DOM is ultimately derived from
habitability. As Ducklow (2002) wrote in the first primary production, and owes some of its chem-
edition of this book: “Oceanic DOM is now rec- ical complexity to it, as phytoplankton generate
ognized as an important component of the bio- enormous molecular diversity at the expense of
geochemical system and possibly a barometer CO2 and just a few inorganic and trace nutrients
of global change.” Accordingly, marine DOM in order to serve their diverse adaptive needs.
research has undergone a renaissance, moving Biochemical processing of primary production
rapidly beyond issues of measurement meth- by genetically diverse bacteria further adds to
odology to critically important spatial-t emporal the chemical complexity of DOM. Intriguingly,
mapping of DOC distribution in the global most of the biomass generated by primary pro-
ocean (Hansell et al., 2009), and now poised to duction is particulate (POM) yet on average
address the underlying regulatory mechanisms. about one-half—but a variable fraction—of
Despite important strides, our understanding primary production becomes DOM within the
of the biogeochemical behavior of marine DOM upper mixed layer, assessed conservatively as
is still in its exciting “early exponential growth bacterial carbon demand. The POM-DOM tran-
phase.” Fundamental questions of the nature sition is a critical step in the flow of reduced
and sources of DOM and mechanisms of its pro- carbon in the global ocean and the capacity of
duction, transformation, and respiration remain the ecosystem to retain elements in the upper
unanswered. So, there is much to do, and there ocean for air-sea exchange; yet we currently
are fresh ideas and powerful new study tools, as lack knowledge of the underlying mechanisms
reflected in this book. Below, I formulate some or the means of direct quantification. There is
problems that I suggest must be solved to un- extensive literature showing that multiple phys-
derstand DOM behavior and to predict the fu- iological, biochemical, and trophic interactions
ture biogeochemical state of the ocean. I hope cause the release of DOM from the particulate
that some young—and not so young—scientists phase—including living organisms. Sloppy
will take on the challenge to solve them. feeding and exudation were long believed to be
The lifetimes of DOM constituents range from the major mechanisms, but with discoveries of
minutes to millennia: some are mineralized rap- new links in the food web there has also been
idly by heterotrophic microbes (labile; LDOM); recognition of additional mechanisms of DOM
others less readily (semi-labile; SLDOM); while production. The list now includes microbial ec-
an incredible diversity of molecules, 1012-1015 tohydrolase activity, viral lysis of phytoplankton
(Hedges, 2002) have accumulated over time to and heterotrophic microbes, cellular release of
comprise the huge (~642 PgC) but intriguing transparent exopolymer particles and other gel
xiii
xiv FOREWORD
particles, programmed cell death, and microbe- transformation of DOM with potential influence
microbe antagonism. It is probable that all on the carbon balance between the ocean and
mechanisms—both those listed and unlisted— the atmosphere. Understanding what renders
cause the POM-DOM transition, but their rela- some of the DOM semi-labile or refractory will
tive quantitative significance varies in time and also require such mechanistic studies. This im-
location. In view of the critical importance of the portant research on dissolved phase carbon cy-
POM-DOM transition for predictive models of cling and sequestration requires new methods,
carbon flow and sequestration in the ocean, I model systems, and concepts (e.g., Microbial
stress the need to develop quantitative methods Carbon Pump; Jiao et al., 2010) addressing in
and a better mechanistic understanding of the situ dynamics and interactions among microbes
production of marine DOM. and (DOM) molecules.
The utilization side of the marine DOM dy- Method refinement has been an important
namics is deceptively simple, since essentially goal in marine DOM research. The field was
all DOM uptake is due to bacteria and Archaea, transformed in the 1990s by the fundamental
the dominant osmotrophic heterotrophs. The discovery that DOM was measurably dynamic,
strength of this coupling is a critical variable in contrary to earlier thinking that the DOM pool
the regulation of DOM utilization and respira- was inert. This discovery “changed every-
tion, and subsequent air-sea exchange of CO . thing.” Interestingly, chemists and microbiolo-
2
Tight coupling also prevents excursions in DOM gists reached this conclusion by different paths.
concentration, so this regulation has major eco- Chemists worked diligently to refine the DOC
logical and biogeochemical implications. How method (in spite of or perhaps because of initial
do microbes manage to biochemically couple setbacks; Hedges, 2002; Sugimura and Suzuki,
so tightly with primary production; and what 1988), achieving ~1 μM precision, sufficient
biochemical and behavioral (e.g., chemokinesis) to show DOC gradients over days to seasons
mechanisms regulate the nature and strength and across locations and depths (Hansell et al.,
of bacteria-organic matter coupling? What is 2009). Marine microbiologists had been finding
14
the role of microbial genetic diversity and bio- as early as the 1960s that C labeled amino acids
geochemical expressions in maintaining the and sugars added to seawater as metabolic trac-
strength of coupling? ers were readily assimilated and respired with
Genomic predictions have provided power- lifetimes of hours to days. Clearly, a DOM frac-
ful constraints. They tell us the molecular inter- tion represented by the radiotracers was highly
actions among DOM molecules and microbes dynamic. Remarkably, the seemingly opposite
that are possible. However, predicting the biogeo- views of DOM lability coexisted for a decade.
chemical dynamics of the complex DOM pool As it turned out, the microbiologists had been
also requires ecophysiological and biochemical observing the behavior of a tiny but dynamic
studies of DOM-bacteria interactions to deter- labile DOM (~1 μM) embedded within an ~40
mine: what DOM transformations do take place, at to 70-fold larger recalcitrant DOM pool. Thus,
what rates, by what biochemical mechanisms, sub- the divergent impressions of the “shape of the
ject to what regulatory forces and in what ecosystem elephant” were due to the enormous range of
context. This is indeed a tall order; but the prob- lifetimes of DOM components. This problem of
lem is critical to solve because of the central role the biogeochemical behaviors of labile and re-
of DOM-bacteria interactions in predicting the calcitrant DOM, and implications for dissolved
carbon cycle of the future ocean. Ocean acidi- phase carbon sequestration, is an active research
fication and warming are likely to affect the area, formalized as the Microbial Carbon Pump
nature and rates of microbial p roduction and (Jiao et al., 2010).
FOREWORD xv
While high precision measurements of DOC a nalytical c hemists, microbiologists and mo-
concentrations (Sharp, 2002) has transformed lecular biologists, and modelers join to address
marine DOM research, further method refine- big questions of carbon cycling and sequestra-
ment and new method development is a high tion, climate predictions, and the biogeochem-
priority. First, achieving 1-2 μM precision still ical state of the future ocean. This multifaceted
requires a magic touch; we need a plug and pursuit has also led to the emergence of modern
play method that even a microbial oceanogra- biogeochemistry as a distinct and dynamic field
pher could use! Second, experimental studies of that is maturing rapidly and attracting students
DOM uptake, respiration, and sequestration re- and postdocs as well as accomplished scientists
quire yet higher analytical precision. An order of from other fields. This advance of marine bio-
magnitude improvement may even enable mea- geochemistry as a discipline responsive to chal-
surements of bacterial utilization of semi-labile lenges posed by climate change may well be
DOC (lifetime 1.5 years; Hansell, 2013) albeit the most important development that has been
requiring long incubations. By analogy, consider stimulated by research on marine DOM.
if the scientists studying ocean acidification Farooq Azam
could only measure seawater pH with precision Scripps Institution of Oceanography
of 0.1 units! (While Dennis Hansell was waiting University of California, San Diego
for me to finally finish this Foreword, X-Prize
worth $2 M was announced for precise and
user-friendly pH instrument: http://www.xprize. References
org/prize/wendy-schmidt-ocean-health-xprize.)
Ducklow, H.W., 2002. Foreword. In: Hansell, D.A., Carlson,
Ultra-precise DOC, DON, and DOP methods C.A. (Eds.), Biogeochemistry of Marine Dissolved
will transform marine DOM biogeochemistry Organic Matter. Academic Press, San Diego, pp. xv–xix.
and climate predictions. Finally, we need a stan- Ducklow, H.W., Doney, S.C., 2013. What is the metabolic
state of the oligotrophic ocean? A debate. Ann. Rev. Mar.
dardized method to measure microheterotro-
Sci. 5, 525–533.
phic (bacteria + Archaea) respiration that does
Hansell, D.A., 2013. Recalcitrant dissolved organic carbon
not significantly perturb the process being ob- fractions. Ann. Rev. Mar. Sci. 5, 421–445.
served. These prokaryotes essentially monopo- Hansell, D.A., Carlson, C.A., Repeta, D.J., Schlitze, R., 2009.
lize DOM and their carbon growth efficiency is Dissolved organic matter in the ocean: new insights stim-
ulated by a controversy. Oceanography 22, 52–61.
low, typically 10-30% (i.e., 70-90% of the labile
Hedges, J., 2002. Why dissolved organics matter. In: Hansell,
DOM-C is respired by heterotrophic microbes).
D.A., Carlson, C.A. (Eds.), Biogeochemistry of Marine
It is currently debated whether or not respira- Dissolved Organic Matter. Academic Press, San Diego,
tion and primary production are in balance or pp. 1–33.
instead display spatial patterns of imbalance Jiao, N., Hernd, G.J., Hansell, D.A., Benne, R., Kattner, G.,
Wilhelm, S.W., et al., 2010. Microbial production of recal-
related to oligotrophic versus meso-/eutrophic
citrant dissolved organic matter: long-term carbon stor-
systems (Ducklow and Doney, 2013).
age in the global ocean. Nat. Rev. Microbiol. 8, 593–599.
The “DOM problem” has been studied for Sharp, J.H., 2002. Analytical methods for total DOM pools.
the better part of a century against significant In: Hansell, D.A., Carlson, C.A. (Eds.), Biogeochemistry
methodological odds, yet significant advances of Marine Dissolved Organic Matter. Academic Press,
San Diego, pp. 35–58.
have been made in the last 10-20 years that
Sugimura, Y., Suzuk, Y., 1988. A high-temperature catalytic
have enriched the field. Today, there is strong
oxidation method for the determination of non-volatile
interdisciplinary convergence and integra- dissolved organic carbon in seawater by direct injection
tion, as marine chemists, organic geochemists, of a liquid sample. Mar. Chem. 24, 105–131.
Preface
Efforts by the ocean science community to un- p hysicochemical sources and sinks; what is the
derstand cycling of the major bioactive elements composition of DOM and how does that illumi-
(C, N, P) in the ocean have experienced great nate elemental cycling? Finally, do we under-
success in the past two decades and continues stand DOM in elemental cycling well enough to
today. Intensive focus on elemental cycling re- accurately represent the processes in models of
sulted from society’s need to determine the role the modern, past, and future oceans?
of the ocean in climate change, in turn requir- In this edition, the progress of the last de-
ing an understanding of its essential functions cade in answering these questions is reported
today, in the past, and in the future. The fun- and synthesized by key contributors to those
damentals of the biological processes involved advances. The book opens with a chapter by
in the transformations of the major elements A. Ridgwell and S. Arndt, setting the paleocean-
have been identified. The next phase of re- ographic context for marine DOM. Study of the
search requires linking the biological processes chemical and isotopic compositions of DOM has
to the very large oceanic reservoirs of the ma- provided unique information on elemental cy-
jor elements, and identifying the sensitivities of cling; both subjects have seen great growth over
those links. Establishing a linkage between pro- the past decade. These works are reviewed in
cesses and reservoirs falls into the discipline of chapters by D. Repeta and S. Beaupre, respec-
biogeochemistry. tively. The biological cycling of the major el-
One of Earth’s largest exchangeable res- ements (C, N, P) through DOM is reviewed in
ervoirs of carbon is dissolved organic matter chapters by C. Carlson and D. Hansell (focusing
(DOM) in the ocean. With a stock of 662 PgC, on biological processes and carbon budgets),
the pool approximates the amount of carbon D. Karl and K. Björkman (focusing on P), and
resident in atmospheric CO2. Prior to the 1990s, R. Sipler and D. Bronk (focusing on N). Particular
this major pool of carbon was primarily evalu- emphasis is placed in these chapters on marine
ated from a geochemical viewpoint; resolving microbes as active agents in the processing of
the biochemical and isotopic composition of the DOM. Photochemical reactivity of DOM, and
pool was a central goal. With an enhanced bio- implications for elemental cycling, is presented
geochemical perspective on DOM, the scientific by K. Mopper, D. Kieber, and A. Stubbins. The
questions began to rest broadly on the role of contributions of optically active (chromophoric)
DOM in the oceanic C, N, and P cycles. Central DOM are covered by C. Stedmon and N. Nelson.
questions were: can we accurately measure The book continues with chapters covering
the concentrations of DOM in the ocean; what DOM at ocean interfaces and in marginal seas
are the distributions of the dissolved organic (i.e., the rivers draining into the ocean, the sedi-
C/N/P pools and what processes controls these ments, the Arctic Ocean, and the Mediterranean
distributions; what are the rates, biogeographi- Sea, in chapters by P. Raymond and R. Spencer,
cal locations, and controls on elemental cycling D. Burdige and T. Komada, L. Anderson and
through the pools; what are the biological and R. Amon, and C. Santinelli, respectively). Topics
xvii
xviii PREFACE
new to this edition include marine microgels, Many individuals and organizations must
introduced by M. Orellana and C. Leck, and be thanked for support of the science that pro-
the long-term stability of marine DOM by vided content for this book, as well as to de-
T. Dittmar. The book closes with the advances of velopment of the book itself. The U.S. federal
DOM in ecosystem and global circulation models agencies supporting much of what has been
by T. Anderson, J. Christian and K. Flynn. reported here, including individual research by
Many in the ocean science community have de- the chapter authors, are the National Science
veloped a strong biogeochemical view of the ocean. Foundation (NSF), the National Oceanographic
This book serves as a tool to provide foundation and Atmospheric Administration (NOAA),
for their forays into the biogeochemistry of marine and the National Aeronautics and Space
organic matter. The book maintains a particular Administration (NASA). The agency pro-
focus on DOM in elemental cycling, and therefore gram managers most important in support-
does not revisit the many, well-d ocumented ad- ing research conducted by the editors are
vances made in organic geochemistry during the Don Rice, David Garrison, and Eric Itsweire
previous decades. Attention is largely to the ma- at NSF, David Legler and Joel Levy at NOAA,
rine environment, with little coverage of the fresh and Diane Wickland and Paula Bontempi at
water systems other than the important rivers and NASA. We greatly appreciate their leadership
dynamics adding DOM to the coastal seas. The and support, and hope they are proud of these
book is directed at professional ocean scientists accomplishments.
and advanced students of biological and chemical
oceanography. Dennis A. Hansell and Craig A. Carlson