A primer on  climate change and microbial life in the ocean
 
Long before humans roamed the planet and the existence of coal-burning power plants, automobiles, plastic bags and iPads, there was the ocean. Then as now, the ocean teems with an extraordinary variation of life forms; coral reefs, blue whales and white sharks, or even a seaside fish market are some sights that come to mind when thinking about life in the sea. Our fascination with sea creatures is not new. It can be traced back almost 2,400 years to the time of Aristotle, when the Greek philosopher would visit fisherman early in the morning to observe and systematically classify marine life, with no more than his naked eye. Unfortunately for Aristotle and the centuries of scientific inquiry that followed him, the naked eye is a woefully inadequate instrument for observing the vast majority of life in the sea.
 
Covering over two thirds of the Earth’s surface and having an average depth near four kilometers, the ocean represents 97% of the planet’s biosphere. Collect a drop of seawater from anywhere in the expansive ocean, present it to Aristotle and he will likely be unimpressed with what he sees. But, mixed with a dye that makes life glow, and gazed at under the microscope, that drop of seawater reveals itself as the habitat of thousands upon thousands of tiny single-celled microorganisms. Multiplied by the volume of the ocean, there are unimaginable 1029 of these microbial cells. Even more surprising, molecular biology techniques have revealed that the ocean’s biodiversity is comprised of untold millions of microbial species. Such profound observations were only made within the last few decades and they turned the field of marine biology on its head. Why are there so many microbial cells in the ocean? How many species are there in the ocean and what governs their distributions? What are they doing? And ultimately, what role do these highly diverse microbial communities play in the ocean food web and global biogeochemical cycles? These are some of the fundamental questions that have inspired marine microbiologists and lead to many exciting discoveries over recent years.    
  
                                                                                                   Microbes and the marine food web
 
In the sunlit top layer of the ocean, plant-like microorganisms called phytoplankton use the energy of the sun to combine carbon dioxide with water, making organic matter and —as a lucky metabolic byproduct— oxygen. Given the size of the ocean, it is perhaps not surprising that we can thank these phytoplankton for supplying half the oxygen we breath here on land. This primary production by phytoplankton is also a cornerstone of the ocean food web analogous to plant production on land. The microbial phytoplankton are consumed by small grazers, who in turn are eaten by others including crustaceans, fish, and ultimately mammals such as whales and the iconic polar bear. This is the classic marine food chain and again we can thank the phytoplankton for providing the carbon that makes up such delicacies as smoked salmon, lobster bisque and seared tuna.
 
Just as plants limit the growth of animals on land, phytoplankton limits the growth of many creatures in the ocean. Growth of phytoplankton themselves is limited. Essential phytoplankton nutrients like nitrogen and phosphorous (ocean fertilizers, if you will) are far from abundant and evenly distributed in the ocean. Consequently, certain regions such as nutrient-rich coastal habitats may seem like terrestrial jungles where primary production is high and can be transferred rapidly to the top of the food chain. Other regions such as the nutrient-poor open ocean may seem at first glance to be more like terrestrial deserts, at least to the naked eye.
 
What happens to all the carbon fixed by phytoplankton and consumed by higher trophic levels? One possibility is that it simply sinks and sits on the seafloor in its various forms ranging from dead phytoplankton to blue whales. But most of it won’t reach the bottom. Why? Because phytoplankton are not the only microorganisms in the ocean. There is a second microbial cornerstone of the ocean food web known as the heterotrophic bacteria and archaea, tiny and diverse cells often simply referred to as bacterioplankton. If you have ever left a head of lettuce or a leg of chicken in your refrigerator while on summer holiday, only to return and find a pool of brown ooze and a rotten stench, then you are already familiar with the role bacterioplankton play in the marine food web. They are responsible for a processes known as remineralization, the breakdown of complex organic matter to carbon dioxide and essential inorganic nutrients. Eventually that brown ooze in your fridge will be completely remineralized too, just give it some more time (or maybe not).
 
So, why doesn’t the ocean stink? Well, in some places it does. At highly productive coastal locales where there are plenty of nutrients, the slow remineralization of macroscopic organisms produces those stinky byproducts of organic matter decay. But, in the massive clear surface waters of the open ocean, primary production is tightly coupled to remineralization; organic matter directly released from phytoplankton is rapidly consumed by bacterioplankton, complicating and limiting carbon and energy transfer up the food chain. Some of the carbon goes into building new bacterioplankton cells, but a great deal of it is returned to the water and atmosphere as carbon dioxide. In effect, the cells “burn” the carbon to produce the energy required for survival and reproduction. At the same time, bacterioplankton play a critical role by regenerating the nutrients required to sustain primary production.
 
The organic matter that does escape recycling at the surface is still transformed by bacterioplankton on its long journey to the deep ocean. Some is remineralized to carbon dioxide, releasing nutrients in the deep ocean. Hence the deep ocean is effectively a rich fertilizer that, when mixed back up into the sunlit surface waters, stimulates phytoplankton growth. Some carbon though is transformed into complex organic compounds that are not accessible to further degradation by bacteria or any living organisms. This recalcitrant organic matter drifting around in the deep ocean is the largest carbon reservoir on Earth. In fact, about fifteen percent of the organic matter produced in the surface ocean is pumped by marine organisms into the deep, where it is “stored” for thousands of years. This biological pump, mediated my microorganisms, can be thought of as a massive carbon processing system that effectively scrubs carbon dioxide from the atmosphere.
 
Interestingly, under the right conditions some of the organic matter will reach the seafloor and become buried. Over millions of years it is transformed into oil, the carbon-rich liquid we use to fuel our automobiles and make our plastics. Hence, over geological time scales primary production at ocean surface has the additional effect of storing carbon deep in the Earth, only to be released en masse by humans later in time.    
           
In this way, phytoplankton and bacterioplankton play a crucial role in the global carbon cycle, the circular path by which carbon flows from the atmosphere into the biosphere, land, ocean and back again. In fact, since the beginning of the 19th century, the ocean has devoured about half of the carbon dioxide emitted from burning of fossil fuels, offsetting accumulation of this green house gas in the atmosphere. Some oceanographers have even estimated that if the microbes in the upper ocean stopped pumping carbon down to the deep sea today, atmospheric carbon dioxide levels would eventually climb another fifty percent from their present state, accelerating global warming further. One is then left to wonder: will the abundance, diversity and activity of these critical microbes be influenced by global warming? And if so, will adaptation of marine microbial communities to climate change accelerate or reduce the impact of global warming? These are difficult, yet pressing questions, in urgent need of answers.    
 
                                                                                 Global warming and phytoplankton

The ocean regulates Earth’s climate. Among other ways, it does so by exchanging heat with the atmosphere, storing it and distributing it around the globe. Consequently, as the atmosphere warms so does the ocean –the surface layer most rapidly. Although far from certain, several studies have predicted the consequences of global warming on marine microbial communities. One line of reasoning goes like this: As the ocean surface warms it becomes less dense and tends to float on top of the cold nutrient-rich deeper water. Without replenishment of the nutrient fertilizer from below, phytoplankton in the warm top layer will starve, leading to reduced primary production and a corresponding decrease in carbon pumping to the deep sea. Is there evidence for this? The answer is yes and it comes from outer space. Scientists can use satellites to measure changes in phytoplankton productivity at a global scale. In doing so over several years, they have shown that sea surface warming in stratified regions of the ocean is accompanied by reductions in productivity. Not good. However, the story is far from that simple. On a perhaps more positive note, primary production may in fact increase at high latitudes as chilly waters warm.
 
Size matters too. Research has shown a significant negative relationship between temperature and phytoplankton cell size. In the Arctic, an ocean facing a particularly large and rapid period of change, the smallest species of phytoplankton are blooming while larger species are wilting away. This phenomenon may also be an adaptation to nutrient availability. Smaller cells have a higher surface-to-area-ratio, providing more effective acquisition of nutrients. The problem though is that large cells sink quickly, smaller ones more slowly. So if projections are true that phytoplankton cell size will decrease with global warming, then we may see a further decrease in carbon pumped into the ocean interior due to a shift to smaller, more buoyant cells. 
 
                                                                                     What about bacterioplankton?

Of all the microbes in the sea, phytoplankton –bedrock of marine food webs–have received the most attention. It also helps that phytoplankton cells, like plants, contain coloured light-harvesting pigments. As we have seen, this attribute has a very practical outcome. Their global distributions can be observed from space, as long as you have the right camera. And, identification, counting and measuring their size in the laboratory is a relatively straightforward and routine task.
 
But what about those essential heterotrophic bacterioplankton? Can we predict their response to a warmer ocean? Maybe, but there is an immense amount of uncertainty associated with the answers. Mostly this is because the critical data on their distributions and activities in the ocean and through time is much more sparse than for phytoplankton. One way of looking at it however, is to treat the bacterioplankton as a microbial black box: organic matter enters the box, carbon dioxide and nutrients exit the box. This bulk process can –and has been– measured for many years and in many places. From these data, the general prediction is that as temperatures rise in the open ocean, this process will tend to increase. Of course it is much more complicated than that, but if true, it seems that in a warmer ocean microbial processes will play an even more important role in the carbon cycle.
 
                                                                  Peering into the microbial black box with genomics

What happens if you open that microbial black box and peer inside? If you use a microscope you will see lots of tiny, mostly indistinguishable cells. If you use molecular genetic tools you will identify many different species. But are all these abundant and distinct organisms doing the same thing? Far from it.
 
In the early 2000’s, marine microbiologists began applying genomics to the study of biodiversity in the sea. By sequencing the DNA extracted directly from the microbes in sea water and analyzing the genes, whole new forms of metabolism were discovered in the ocean. In a now classic study, scientists discovered genes for phototrophy –the process of harvesting energy from light– in bacteria that were previously assumed to rely exclusively on organic matter for energy. Even more seemingly exotic metabolisms have since been discovered in the sea. For example, there are bacteria in the ocean that use noxious hydrogen sulfide as an energy source, and archaea that use the waste product ammonia in the same manner. Both may use organic matter as a source of carbon, but can also fix carbon dioxide in much the same way that phytoplankton do. These studies and others have demonstrated that bacterioplankton play a much greater and more complicated role in marine food webs than simply breaking down organic matter and recycling nutrients to phytoplankton. The challenge now is to understand how such  newly discovered microbial life forms fit into the marine food web and influence biogeochemical cycles. Until we know that, we can only speculate on how they are influenced by climate change. 
 
                                                                                   Microbes as sentinels of change

The microbial world is often left out of discussions of climate change. Perhaps because these tiny creatures are not as obvious to us as polar bears or blue whales. Or not as economically important as salmon or tuna. But as critical players in the carbon and other biogeochemical cycles, their responses to climate change demand our attention. More worrying though, climate change is not only leading to a warmer ocean, but an ocean that is changing in other profound ways. Carbon dioxide accumulation is leading to ocean acidification. Oceanic stratification is resulting in the expansion of oxygen-depleted dead zones. At present, the jury is out on how microbial food webs and biogeochemical cycles will be influenced by these fundamental changes to Earth’s largest ecosystem.
 
As a final note, studies are now beginning to show that marine microbes may be harbingers of change and could serve as sentinels by which we can monitor climate change effects on marine ecosystems. If so, then there is a critical need for long term time-series of biological measurements of marine environment if we are to accurately predict change. Indeed, we may have come a long way since Aristotle, but much about the microbial ocean remains a mystery.