Microbial Oceanography: the Challenge of the Sea: Berne, 12.11.2015 Forum (vidéo + texte – anglais)

États-Unis

David Karl

Prix Balzan 2015 pour l'océanographie

Pour ses contributions fondamentales à la compréhension du rôle et de l’importance des microorganismes dans l’océan et du contrôle que ces derniers et le phytoplancton exercent sur les cycles océaniques du carbone, de l’azote et du fer. Ses travaux ont fourni des éclaircissements significatifs sur les changements climatiques.

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Microbial Oceanography: The Challenge of the Sea

Introduction

The ocean covers nearly 71% of the surface of our planet, yet remains one of the least well explored habitats on Earth. As an integral component of the climate system, oceans store and transport heat, produce and consume climate-reactive gases and regulate the hydrological cycle of the planet. Fossil fuel consumption, land use changes and other impacts of a manufacturing-based global society have begun to stress and alter the delicate balance of life in the sea. It is essential that we develop a comprehensive understanding of the structure and function of these complex marine ecosystems and use this knowledge to preserve and sustain their natural state. Beyond this contemporary challenge of the sea is the anticipation and uncertainty of the future.

Microorganisms inhabit all marine ecosystems, from the tropics to sea ice and from the sunlit surface ocean to the dark abyss. They harvest solar energy, catalyze key transformations of matter, produce and consume most greenhouse gases and serve as the base of the marine food web. Microorganisms have always dominated our planet, and always will. For example, there are more microbes (bacteria, archaea, protozoa and viruses) in 1 liter of seawater – approximately 10 billion – than there are people on Earth. And this large and diverse assemblage is metabolically active, with a daily ocean-wide power expenditure nearly 50 times greater than that of the world’s global economy. As Louis Pasteur correctly proclaimed, “the very great is achieved by the very small.”

Modern studies in oceanography, the scientific study of the sea and its inhabitants, can be traced back to the worldwide voyage of Her Majesty’s Ship Challenger. During that historic, 4-year expedition, and on subsequent scientific voyages through the first half of the twentieth century, a basic understanding of the structure and function of the marine environment was obtained. However, many fundamental discoveries were yet to come; for example, the theory of plate tectonics, the discovery of deep-sea hydrothermal vent ecosystems and the immense role that marine microorganisms play in sustaining planetary habitability.

I am extremely grateful to the Balzan Foundation for selecting the field of Oceanography for the prestigious 2015 Balzan Prize, and humbled to have been chosen to represent the discipline on this occasion. The great honor is even more significant for me because one of the most influential and inspirational oceanographers of the 20th century, Roger Revelle, also received the Balzan Prize in Oceanography in 1986. Among his many achievements, Revelle built an extensive fleet of research vessels to provide access to the sea and initiated studies of the ocean’s carbon cycle. Like Revelle, my own research has been largely field-oriented with a focus on microbial biogeochemistry, including carbon and associated bioelements.

My Voyage Through Life in Science

In 1960, the well known author, scientist, philosopher and futurist Sir Arthur C. Clarke wrote a book entitled The Challenge of the Sea. I have borrowed that title for my own presentation today because there are still many scientific challenges as well as many opportunities in the field of oceanography. Clarke told the story of our new underwater frontier and speculated about the tremendous impact that the sea will have on our lives in the future. At the influential age of 10 years old, I was captivated by the great potential for scientific discovery and motivated by Clarke’s “Challenge of the Sea.” I knew right then and there that I wanted to become an oceanographer and now, more than 50 years later, I am still pursuing my dream.

In 1972, I enrolled in graduate school at Florida State University and after just one semester I participated in my first oceanographic voyage. This expedition, from Curaçao to Jamaica via the Cariaco Trench, focused on the chemistry and microbiology of an unusual deep-sea anoxic marine habitat that had been discovered only a few decades earlier. I continued my education and oceanographic fieldwork at Scripps Institution of Oceanography, and in 1976 participated in my first expedition to Antarctica. Following graduation in 1978, I moved to the University of Hawaii to begin my new career in academia. Collectively, I have spent more than 1,000 days at sea, making observations and conducting experiments in numerous habitats worldwide. Selected research waypoints include the Black Sea, Amazon River estuary, North and South Pacific gyres, Guaymas Basin, Gulf of Mexico and 23 expeditions to Antarctica (Figure 1). My lifelong interest has been in the study of the microbial inhabitants of the sea, their biodiversity and controls on metabolism and growth. Because marine microorganisms were the first life forms to appear on our planet, they have a nearly 4-billion-year evolutionary history, and over time their metabolism has fundamentally changed the chemistry of the sea and our atmosphere, making it possible for the rise of terrestrial life, including humans.

A Sea of Microbes: New Views on an Old Ocean

Microbial oceanography is a relatively new discipline that integrates the principles of microbiology, microbial ecology and oceanography to study the role of microorganisms in the biogeochemical dynamics of natural marine ecosystems. Research conducted mostly during the past half-century has built a coherent, conceptual understanding of the role that microorganisms play in the general economy of the sea.

A general goal of microbial oceanography is to observe and understand microbial life in the sea well enough to make accurate ecological predictions, for example, of the impact of climate variability on microbial processes in the global ocean. By analogy to a living cell, the ocean has a collective metabolism that is based largely on its dynamic genetic blueprint, with expressed phenotypes that control fluxes of energy and matter. The microbial processes that underlie this collective metabolism are influenced by environmental forcing, including anthropogenic impacts.

Despite the fact that marine bacteria are the oldest forms of life on our planet, with origins nearly 4 billion years ago, they were not discovered until the invention of the microscope. The earliest study of marine microorganisms dates back to the mid-17th century. The Dutch textile merchant and amateur lens maker Antony van Leeuwenhoek was the first to report in 1677 what he termed “little animals” in seawater. However, neither van Leeuwenhoek nor his contemporaries had any understanding of the nature of these tiny, microscopic life forms. It would be another 150 years until the Prussian microscopist Christian Gottfried Ehrenberg (1795-1876) and others conducted detailed laboratory studies of marine microorganisms and established their proper place in the hierarchy of life on Earth. The first golden age of microbiology quickly followed with detailed studies of bacterial growth, infectious disease and pathology, vaccination and immunology and the science of microbial fermentation. Leaders during that period included Ferdinand Julius Cohn (1828-1898), Robert Koch (1843-1910) and Louis Pasteur (1822-1895), perhaps the greatest microbiologists in the history of science.

However, it would take another half-century before systematic studies of the microbial inhabitants of the sea and their crucial role in global ecology began. Medical and industrial microbiology were important predecessors to microbial oceanography and microbial ecology. While these otherwise disparate fields shared some basic methodologies, novel approaches would also be required to move marine microbial science forward. Measurement of fundamental properties of marine ecosystems such as total microbial biomass, rates of growth and pathways of energy flow were the contemporary challenges of that period (ca. 1960-1975). By the time I received my Ph.D. degree in 1978, we thought that our understanding of microbial processes in the sea was fairly complete, and I seriously considered moving into a different field of study, one that might provide greater challenge and opportunity. However, one could never have predicted the fundamental discoveries that were about to be made. This new knowledge transformed our view of microbial life in the sea and led to the creation of a new scientific discipline, microbial oceanography, one that combined the principles of microbiology, ecology, biogeochemistry and oceanography into a holistic science of microbial life in the sea.

During my first year in Hawaii, I participated in an expedition to the recently discovered deep-sea hydrothermal vents on the Galapagos Rift, and published one of the first papers on the microbial basis for animal life in these unprecedented ecosystems. Within the next decade, the most abundant photosynthetic life form on Earth, a microscopic marine cyanobacterium, was discovered (Table 1). This challenged our paradigms and reminded us that our ignorance of microbial life in the sea probably exceeded our extant knowledge. These were very exciting times indeed. A few years later, a third domain of life, the marine planktonic archaea, were discovered and found to be a dominant life form in deep marine ecosystems. Additional, fundamental discoveries of new organisms, new metabolic pathways and novel strategies for survival were also reported. One of the more unexpected and probably most significant discoveries to date was that of a novel pathway for the transformation of sunlight into useful biological energy (Table 1). This ubiquitous solar energy capture mechanism involves a photoactive membrane protein, proteorhodopsin, that functions as a sunlight-driven proton pump that is coupled to the production of ATP, the universal energy currency of all living organisms. So in effect, microbes in the surface ocean function as an enormous solar panel to supplement the solar energy that is captured through the more well-known process of green plant photosynthesis. We are just beginning to explore the quantitative significance of the proteorhodopsin – solar energy flux pathway.

Many of these discoveries were facilitated by new DNA sequencing technologies developed for the human genome project. Collectively, this rapid progress in the field of microbial oceanography during the past few decades legitimately qualifies as the second golden age of microbiology, on par with the fundamental discoveries of Pasteur and others more than a century before.

The Origin of Life on Earth and the Imprints of Microbes and Humans

Planet Earth, our home, has been more than 4.6 billion years in the making. If we view Earth’s history in the form of a 24-hour nautical clock, we can identify several important benchmarks (Figure 2). An initial cooling phase, lasting more than 500 million years, created the continents and the ocean. Then, more than 3.5 billion years ago life arose in an ancient ocean at about 0500 hr on our Earth history clock, just before dawn.

The first life forms – single-celled microorganisms – evolved in an early ocean that was sulfide- and iron-rich, and free of oxygen. These conditions persisted for hundreds of millions of years until the process of oxygenic photosynthesis transformed the planet, starting at about 0820 hr. This was one of the most fundamental benchmarks in our planet’s history. Among other consequences, the advent of oxygen on Earth enabled the evolution of the first eukaryotes, also single-celled microorganisms, just after 1500 hr. However, it was not until much later, nearly 2100 hr, or 4 billion years after Earth’s formation, that simple eukaryotes evolved into larger, more complex life forms and moved onto the land. Despite the diversity of life that evolved during our planet’s history, it began and still is dominated by microorganisms and, as Arthur C. Clarke noted, “all life came from the sea and most of it is still there.” Incredibly, modern humans (Homo sapiens sapiens) did not appear on Earth until about 200,000 years ago, and the period since the start of the Industrial Revolution represents a few milliseconds on the 24-hour clock of Earth history. It is amazing to think what humans have achieved during this brief time on Earth – both good deeds and evil.

Tracking Carbon Dioxide from Fossil Fuel to Ocean Acidification

Mauna Loa, Hawaii, was selected as the site for one of the first observatories to track atmospheric concentrations of carbon dioxide (CO2), with Roger Revelle playing a major role in this effort. In his 1957 Tellus paper with Hans Suess, Revelle set out to measure the residence time of CO2 in the atmosphere. Based on the best information available at that time, they concluded that “the average lifetime of a CO2 molecule before dissolution into the sea is on order of 10 years.” Revelle and Suess warned that “human beings are now carrying out a large-scale geophysical experiment of a kind that could not have happened in the past, nor be reproduced in the future” (Figure 3). This experiment, one of humankind’s doing, was an opportunity to learn more about the coupled ocean-atmosphere system, and Revelle set out to do just that during the 1957–1958 International Geophysical Year (IGY).

Revelle, who chaired the US National Committee for IGY, and other scientists made a strong case to the committee regarding the value of making baseline atmospheric CO2 measurements against which future change could be measured. To accomplish this goal, Revelle – who was at that time also Director of Scripps Institution of Oceanography – hired Charles David Keeling, then a postdoctoral fellow at Caltech. Initial measurements obtained in 1958 atop Mauna Loa, Hawaii established a baseline CO2 concentration of approximately 315 parts per million (ppm). The concentration has risen, year after year, to current levels of ~ 400 ppm. This well-calibrated, atmospheric time series is an indelible imprint of humans and an ominous warning of the future state of our planet in a business-as-usual scenario.

Because the ocean plays a central role in regulating global atmospheric CO2 concentration, there was a great interest in the establishment of one or more ocean observatories to improve our understanding of the oceanic carbon cycle. In addition to investigating the exchange of CO2 between the atmosphere and the open ocean, these oceanic time-series stations could serve as representative, benchmark sites to develop an understanding of the entire carbon cycle from controls on photosynthesis and respiration to rates of long-term sequestration of carbon and associated bioelements into the deep sea. These processes, collectively termed the “biological carbon pump” are predominantly controlled by microbes. This new information would then be used to inform global models that would develop a capability to predict, on a global scale, the response of oceanic biogeochemical processes to anthropogenic perturbation, in particular related to human-induced climate change. This was a tall order, a challenge for the ages but also an enormous opportunity to promote the new discipline of microbial oceanography.

By fall 1988, two open ocean observatories, one in the North Atlantic near Bermuda and the other in the North Pacific near Hawaii (Figure 4), were established. These stations provided global reference points for tracking the ocean’s health, including but not limited to measurements of atmospheric CO2 invasion and ocean acidification (Figure 5). The Hawaii site, Station ALOHA (A Long-term Oligotrophic Habitat Assessment) has been studied on an approximately monthly sampling schedule for the past 28 years. It has become a global laboratory for trans-disciplinary scientific investigations of microbial oceanography, a site for hypothesis testing, ecosystem experimentation and an oceanic university for training the next generation of leaders.

Station ALOHA is one of only a few open ocean locations where ongoing time-series observations are being conducted. This ocean surveillance program is predicated on the straightforward assumption that certain processes, such as species succession and climate variability, are long-term processes and need to be studied as such. Every month since October 1988, teams of scientists have visited Station ALOHA to observe and explore a variety of parameters. The physical and chemical characterization of the habitat is as important for our understanding of microbial processes as the microbial assemblage itself. The most basic and relevant information about sea microbes includes community structure and organization, distributions, abundances and in situ metabolic activities as well as the ecological controls thereof. As time-series data accumulate, new phenomena previously hidden in the “invisible present” become apparent and new understanding emerges.

During the first 20 years of observations at Station ALOHA, we established a long-term climatology of microbial and biogeochemical processes, a baseline against which future change from this mean state can be assessed. However, any time-series observation program, regardless of when it began or how long it has been active, is only a snapshot of the complex time-space domain of natural environmental variability and change upon which human impacts are superimposed. It has been demonstrated that for systems in which the signal-to-noise ratio is low, unambiguous detection of climate change effects on microbial processes at Station ALOHA and similar oligotrophic marine environments will probably require at least 30-40 years of systematic observation. This sobering assessment of the scale of the challenge of the sea further incentivizes ocean observation programs like those conducted at Station ALOHA.

Science, Society and Sustainability

In The Challenge of the Sea, Clarke predicted a future where the ocean would become an increasingly important source of food, energy and natural resources. These multiple uses of the sea for societal benefits oftentimes compete with natural processes and may have unintended ecological consequences. Can we afford the risks, manage the vulnerabilities and adapt to human-induced climate change?

To assess these important questions, the United Nations established the Intergovernmental Panel on Climate Change (IPCC) in 1988. Its mission is to provide a comprehensive scientific assessment of the world’s climate. The assessment process and periodic written reports are objective, transparent and based on the most up-to-date scientific, technical and socio-economic data. The reports cover the physical basis of human-induced climate change, potential impacts and societal options for adaptation and mitigation. IPCC reports are policy-neutral, but policy-relevant. To date, five assessment reports have been completed (1990, 1995, 2001, 2007, 2013-14). Assessment Report #5, Working Group II contained two new chapters on the state of the ocean and concluded that “The ocean is changing.”

While CO2-induced ocean acidification has received the most attention, there are several additional stresses on marine ecosystems that are more difficult to observe and impossible to predict. For many of these processes, including microbial biodiversity and metabolism, there is no baseline from which to track future states. Furthermore, warming and sea-ice melting will cause enhanced stratification of the surface ocean, leading to changes in ocean circulation, upwelling and a reduction in the flux of essential nutrients to sustain photosynthesis. Deoxygenation of coastal marine ecosystems from excess nutrient runoff and the gradual loss of oxygen in the atmosphere (and eventually the ocean) due to fossil fuel burning will impact microbial and metazoan metabolism and also lead to a reduction in ecosystem productivity.

Human-induced climate change alters marine ecosystems in a complex manner due to multiple synergistic and antagonistic stressors acting on a variety of space and time scales. Some ecological processes have thresholds or tipping points beyond which they become vulnerable to collapse. A relatively new branch of ecology is attempting to develop the theory and observational framework to identify leading indicators of ecosystem change. For example, wider swings in dynamics of key variables, slower return rates following natural perturbations and shifts in parameter variance towards lower frequencies have been identified as possible leading indicators to major ecosystem change. However, all of these require the establishment of a program to observe the dynamical behavior of the ecosystem and changes in key variables over time. Global simulations must embrace the interactive, dynamical conditions of natural systems to obtain meaningful predictions of future ecosystem states. This is an enormous contemporary challenge of the sea.

Human Perturbation to the Global Nitrogen Cycle: A Case Study

The global cycle of nitrogen (N), an essential element for all living organisms, is controlled primarily by the balance between two major microbiological processes: nitrogen fixation (NF) which adds biologically available N (also known as fixed N), and denitrification which removes available N. The process of NF involves the conversion of the nearly unlimited supply of nitrogen gas (N2) which cannot be used directly as a nutrient, into ammonia, a readily available form of N. NF is performed by a small group of specialized terrestrial and marine microorganisms whose metabolism and growth in the surface ocean is regulated, in part, by the availability of phosphorus (P), another essential nutrient for all living cells. As P becomes limiting, the supply of new ammonia to the ecosystem via NF is curtailed and productivity decreases. Over time, P begins to accumulate due to net remineralization of organic matter and upward diffusive transport of P from the deep sea. The dynamical balance between the net change in available N (difference between NF and denitrification) and the delivery of P in open ocean habitats like Station ALOHA structures the microbial community and sets constraints on productivity and other ecosystem processes, including CO2 sequestration.

In the early 1900s, the German chemist Fritz Haber invented a process whereby ammonia could be synthesized chemically from N2. With subsequent commercialization of this novel process, humankind now had access to an inexhaustible supply of ammonia for use in fertilizer manufacturing to enhance soil fertility and crop yields and for a variety of additional industrial purposes. By 1980, the annual rate of human industrial NF surpassed the pace at which nature had previously supplied fixed N to the planet (Figure 6). This has led to N pollution of our waterways and selected coastal marine environments, and to a cascade of unintended ecological consequences including blooms of toxic phytoplankton and the formation of “dead zones.” More recent studies have also shown that fixed N concentrations (and the fixed N:P ratios) in the surface waters of the North Pacific Ocean downwind of fast-growing economies of northeast Asia have increased significantly since 1970. We hypothesize that this excess N, produced by humans, will eventually decouple the oceanic N and P cycles, leading to P stress, fundamental changes in microbial community structure and a general destabilization of the marine biosphere. Recent global surveys indicate that this manmade N pollution may have already reached the remote central regions of the North Pacific Ocean. Ongoing ocean time-series observation programs such as Station ALOHA will be invaluable for tracking N pollution and the attendant ecological consequences. This case study is just one example of the challenges we face in our efforts to sustain both our global economies and the sustainability of our planet.

Prospectus for the Future

The contemporary challenge of the sea is enormous, and there is an urgent need for more scientists in a complex and changing world. Our future will also benefit from a greater public understanding of the sea around us, and new policies to conserve our limited natural resources.

Microorganisms have helped to shape the physical, chemical and biological state of planet Earth. In open ocean ecosystems, planktonic microbes dominate the living biomass, harvest light energy, produce organic matter and the oxygen we breathe, and facilitate the storage, transport and turnover of key bio-elements, especially carbon. While these activities are key to Earth’s habitability and sustainability, available observations, theory and models that integrate microbial influence on biogeochemical, ecosystem and climatic processes still need to be developed. The discipline of microbial oceanography has experienced remarkable growth in my scientific lifetime. The discoveries of novel microorganisms, unexpected metabolic processes and fundamental ecological and evolutionary relationships have challenged extant paradigms and created new and exciting research opportunities.

There are numerous global scale challenges that are inextricably linked to the burgeoning human population, industrialization and climate change. In order to move forward with solutions, we must have a meaningful, comprehensive understanding of ocean habitat variability and biodynamics, including prognostic modeling of future ecosystem states. Without this information, we increase the risk of making grievous errors in management and policy decisions that may impact the current and future health of our ocean ecosystems and all that they support. Furthermore, we need to communicate this information broadly to society and include it in contemporary academic and community informal educational programs to increase public awareness about the importance of the research and to contribute to personal career choices, accountability and policymaking.

It is impossible to predict future research directions in microbial oceanography where unexpected discoveries of major significance are commonplace. Without a doubt, this is a great time to be a microbial oceanographer, with numerous challenges and great opportunity. By combining novel and rapidly evolving molecular methods with more traditional techniques in microbiology, oceanography and ecology it may be possible – for the first time – to address fundamental questions and to develop a meaningful predictive understanding of the ocean with respect to energy transduction, carbon sequestration and bioelement cycling and their relationships to habitat variability and climate change. My Balzan Prize will provide support for two early career microbial oceanographers, one from Italy and one from Spain, who will join an international, trans-disciplinary collaboration to address these fundamental challenges of the sea. The synergy created by engaging experts who traditionally have not worked together has mutual benefit for science and for society. It should be an exciting and productive next decade.