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Tiny Climate Changers

Marine plankton

Ecological processes among microscopic marine plankton can influence chemical cycling processes that ultimately control climate at the global scale.

By Justin Seymour

Marine microorganisms have profound impacts on the chemical cycling processes that influence global climate. Now their behaviours and preferences have been captured on video.

They may not be as conspicuous as fish, sharks and whales, but microbes are by far the most abundant organisms in the ocean. A teaspoon of seawater typically contains more than one million bacteria, which equates to more than 1028 bacteria across the global ocean. These bacteria are also extremely diverse, with recent estimates suggesting that a single bucket of seawater will host more than 25,000 different bacterial species.

The ocean’s community of microorganisms also includes the zooplankton, which are microscopic animals that form the base of the marine food chain, and the phytoplankton, which are the microscopic algae responsible for approximately half of all photosynthesis on Earth.

This rich and diverse community of planktonic microbes represents the foundation of the marine food web, and is therefore essential for supporting the productivity and function of the entire ocean.

These microbes are also the driving force behind many of the ocean’s major chemical cycles, including the carbon, nitrogen and sulfur cycles, which are not only essential for the survival of all life in the ocean but have a strong and direct impact on global climate.

The Microbial Seascape
For more than 100 years, oceanographers have studied marine processes by embarking on surveys where measurements and observations are made across distances ranging in scale from hundreds of metres to kilometres. Today, with the aid of satellite imaging technology, we can easily measure physical and biological patterns in the ocean across thousands of kilometres.

However, for the tiny planktonic microbes inhabiting the surface of the ocean, life is defined on much smaller scales. These marine microbes inhabit a microscale world where their food, their competitors and their predators are distributed across a complex and patchy seascape that can be encapsulated within a fraction of each individual drop of seawater.

To exploit this microscale seascape, many microbes can swim through their liquid environment in search of resources and favourable niches, and often use ecological strategies that mirror those of larger organisms. However, microbes lack higher senses such as vision, and must therefore use more simplistic approaches for finding food, prey or mates.

One of the most important and widespread strategies employed by microbes is the ability to sense and direct movement in response to chemical signals. Dilute pulses of various chemicals, dissolved in seawater, can represent important sources of food and nutrients for bacteria and phytoplankton, or cues for the presence of prey or mates for zooplankton. By directing their movement in response to the gradients of these chemicals – a behaviour known as chemotaxis – microbes can subsequently migrate into favourable microenvironments where their access to resources is enhanced.

Microbes and the Ocean’s Sulfur Cycle
As well as using dissolved chemicals as behavioural cues and resources to grow, marine microbes are the central players in the complex network of chemical cycles that maintain the ocean’s chemical balance, which is essential for controlling our planet’s climate. By performing a near-endless array of diverse chemical transformations, marine microbes represent the engine-room of ocean chemical cycling.

One of the major chemical cycles in which marine microbes play a fundamentally important function is the ocean’s sulfur cycle. The role of planktonic microbes in this cycle is largely centred around an organic sulfur compound called dimethylsulfoniopropionate (DMSP), which is produced by several species of phytoplankton and plants. DMSP is used by phytoplankton as an osmolyte – a substance used to maintain cell volume and fluid balance within a liquid environment. It is now clear that DMSP also plays an important role in the ocean’s chemistry and ecology, and even shapes the complex processes that affect our weather.

When DMSP is produced by phytoplankton it has two fates that are largely governed by the activities of other microbes. Like other organic molecules produced by phytoplankton, DMSP is an important growth resource and contributes up to 10% of the carbon and nearly all of the sulfur requirements of marine bacteria.

However, it has recently become clear that not all ocean bacteria use, and cycle, DMSP in the same way. This has important implications for marine sulfur cycling.

Many species of marine bacteria consume DMSP and directly assimilate the sulfur into proteins. However, some other groups of bacteria degrade DMSP in a manner that releases another compound called dimethyl sulfide (DMS). This is significant because DMS is the major way in which oceans emit sulfur into the atmosphere, and is thus a pivotal component in the global sulfur cycle.

Once in the atmosphere, DMS is rapidly oxidised into aerosol sulfates, which act as cloud condensation nuclei that absorb and scatter incoming sunlight. This alters the atmospheric heat budget and thus influences global temperatures. Cloud condensation nuclei are also involved in the formation of clouds, which further influences regional weather patterns.

The balance between the two competing pathways of DMSP degradation, which is largely determined by the activities of diverse marine bacterial populations, can influence the amount of DMS that is released from the ocean into the atmosphere and subsequently influences our climate. Seasonal and annual variability in the release of DMS can also be directly linked to shifts in chemical cycling processes involving marine plankton.

DMSP as a Behavioural Cue
As well as playing an important role in ocean microbiology and the global sulfur cycle, DMSP and related compounds, including DMS, appear to be important chemicals in the ecological interactions of several marine animals. These chemicals are potent behavioural stimuli for foraging marine invertebrates, fish, birds and mammals, which may use DMSP and DMS as cues for finding food.

However, the role of these chemicals as behavioural cues for the microscopic organisms that are responsible for producing and recycling them is not so clear. Previous evidence indicates that some bacteria may be attracted to DMSP, while other studies have suggested that DMSP may actually be used in a chemical defence mechanism by some phytoplankton to ward off potential zooplankton grazers.

So that we can more precisely understand the mechanisms behind DMSP and DMS cycling, it is important that we acquire a clearer understanding of how these chemicals fit into the microbial ecology of the ocean.

Measuring Microbial Behaviour and its Role in Sulfur Cycling
To examine the ecological role of DMSP in the marine microbial food web, we have developed a system that enables the study of microbial behaviour at the very small scales over which microbes forage within ocean environments. This has allowed us to begin to study microbial ecological interactions directly, in the same way that ecologists study the behaviour of larger organisms. To achieve this, we have manufactured a microfluidic device that generates microscale pulses of DMSP to mimic the release of this compound into seawater.

Microfluidics is a new technology that involves the design and fabrication of very small chips that incorporate precisely etched channels and microscopic features that enable the accurate control of very small volumes of fluid. Within these devices, chemical gradients can be generated and the behavioural interactions of microorganisms can be directly studied within a controlled experimental setting.

The device used in our experiments comprises a single 3 mm-wide channel filled with suspensions of various species of swimming marine microorganisms. Within the channel a microinjector injected a band of DMSP into the microbial suspension. This generated a diffusing pulse of DMSP mimicking what is likely to occur in the ocean after a phytoplankton cell leaks DMSP into the surrounding water or is killed following viral infection or grazing by zooplankton. We then used a video-microscopy system to directly track the swimming behaviour of a range of organisms, including several species of marine bacteria, phytoplankton and zooplankton.

Our results indicate that, in the same way that it represents a behavioural stimulus for higher organisms, DMSP is used by many marine microbes as an important foraging cue.

We found that two species of marine bacteria were rapidly attracted to pulses of DMSP in our microfluidic channel. Upon detecting DMSP, the bacteria immediately swam into the patch and remained inside it in a tight cluster of cells for several minutes. This behaviour allowed these chemotactic bacteria to enhance their exposure to DMSP by up to 66%.

Considering the rich source of carbon and sulfur provided by DMSP, this behaviour could provide a significant competitive advantage in the environment. Furthermore, by determining which bacterial populations gain first access to ephemeral pulses of DMSP, these behavioural responses may ultimately control how much DMS is produced. Interestingly, we found that some phytoplankton species that do not produce DMSP showed similar behavioural responses.

In our experiments, two out of three phytoplankton species showed strong chemotactic responses to DMSP and DMS, and rapidly swam into the microscale patches in the same manner as the bacteria. This provided one important species, Micromonas pusilla, with a 41% increase in exposure to DMSP, which it assimilated to use its sulfur for growth.

Finally, we examined the response of two species of microscopic zooplankton to DMSP patches. Like the bacteria and phytoplankton, both species exhibited strong foraging responses to the DMSP and DMS. One species, Oxyrrhis marina, rapidly and directly migrated into DMSP patches. Once inside the patches, it significantly modified its swimming behaviour by turning more frequently to maintain position its within the patch. Oxyrrhis marina is a voracious consumer of DMSP-producing phytoplankton, and we expect that it employs chemotactic responses to DMSP to hunt for prey cells in the environment.

Implications in the Ocean
Our experiments indicate that, in the same way as they are behavioural cues for larger marine organisms, including fish, birds and mammals, DMSP and DMS are important chemical signals for swimming marine microbes. Diverse marine microbes, spanning three levels of the planktonic food web, exhibited strong behavioural responses to these chemicals.

These responses will provide enhanced exposure to the chemicals required for growth (carbon and sulfur) for bacteria and phytoplankton, as well as potential chemical cues for the presence of prey for zooplankton. Such behavioural responses will also influence competitive interactions between different populations of marine microbes, which will ultimately influence DMS production.

This means that ecological processes among microscopic marine plankton, played out across sub-centimetre scales, can influence chemical cycling processes that ultimately control climate at the global scale.

Justin Seymour is a Research Fellow at the University of Technology, Sydney.