American Society of Naturalists

"Evolution Promotes Resilience of Marine Mixotrophic Metabolic Strategies to Thermal Stress"

Kevin M. Archibald, Stephanie Dutkiewicz, Charlotte Laufkötter, and Holly V. Moeller: Read the article

Microbes are everywhere. They are organisms invisible to the naked eye, but their populations and communities pack a punch far beyond their size when it comes to ecosystem health. In our oceans, changes in microbial communities often signal, or even drive, broader ecological shifts.

Temperature changes in our oceans and marine systems occur across a wide range of timescales. Daily cycles, like the difference between day and night, are examples of short-term fluctuations. Seasonal changes over months and longer-term trends, such as rising average temperatures over decades, represent more sustained thermal pressures. Microbes have certain temperatures in which they grow fastest, but when temperature fluctuates, growth challenges arise. Strategies that microbes use to account for both short- and long-term fluctuations can be both genetic and metabolic. A recent study by Archibald et al. investigates how temperature stress and fluctuations affect the adaptation of a special group of microbes called mixotrophs. Mixotrophs are unique because they can harvest energy in multiple ways: through photosynthesis, grazing other organisms, or by combining both strategies. This flexibility allows them to thrive in dynamic environments—a trait that’s increasingly important as climate change disrupts ocean temperatures. But how does thermal variation affect the metabolic strategies accessible to mixotrophs?

Prior experimental work by Dr. Moeller’s group (Leprori-Bui et al.) showed that mixotroph evolution can help microbes deal with thermal stress. However, the limits to this evolution remained unknown. When considering evolution, the authors focus on genetic changes that increase an organism's fitness, here described as the rate of cell divisions. For example, a change in a gene from parent to offspring that allows a protein to increase its optimal temperature. However, genetic changes like these that are necessary for evolution take many generations to impact the fitness of a population. So, what about the short-term temperature shifts we talked about earlier? The good news is that evolution is not the end-all be-all of mixotroph responses! They can more rapidly change their traits via phenotypic plasticity. Phenotypic plasticity is the ability of an organism to change its metabolism without needing to undergo several reproductive events. Phenotypic plasticity can occur within hours to days in microbes and it is generally how microbes respond to short-term temperature variations.

To understand how the aspects of mixotrophy (grazing, photosynthesis, a combination) respond both genetically and metabolically to different temperature variations, the researchers developed a dynamic mathematical model of a mixotroph population. By studying how the simulated population changed its overall investments in photosynthesis, grazing, and reproduction in response to temperature shifts, the researchers found that varying the metabolic strategies through plastic and genetic changes help mixotrophs deal with the stress of changing temperature conditions. While short-term metabolic responses to temperature changes can be very large, over long time-scales evolution helps mixotrophs return to normal even if the temperature remains high. This stability in metabolic strategy over evolutionary timescales shows a strong resilience in the mixotrophic lifestyle, potentially minimizing disruption to ocean carbon cycling.

Note that the level of warming simulated (6 degree Celsius) is extreme when compared to predicted global average temperature changes (0.5-2 degree Celsius), but represents realistic heat waves that can last for over a year in some cases. Single-celled organisms like mixotrophs evolve quickly (timescales of hundreds of days), so these evolutionary and metabolic effects play out during heat waves as well as centuries-long warming trends.

Future expansions to this work could consider how multiple successive warming events, changes to evolution or phenotypic plasticity rates, and community dynamics (resource competition) might impact the strategies that mixotrophs will use to contend with a warming ocean.

As oceans continue to warm, mixotrophs may be among the microbial world's most agile survivors, shape-shifting strategists at the heart of marine food webs. Ubiquitous and crucial, the ability to account for changes in their traits due to temperature changes will expand our understanding of changing oceans for microbial generations to come.

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Hagen Klobusnik is a second-year PhD student in the Kremer Quantitative Ecology and Evolution Lab at the University of Connecticut. Their research focuses on aquatic microbial population and community dynamics in temporally variable environments, combining mathematical modeling and empirical data. When not thinking about cool science they can be found weeding their garden, hiking under tall trees, or reading hard science fiction books.