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To understand ocean's microbes, look at their metabolism
By Stilianos Louca. September 9, 2016

In contrast to larger organisms such as plants and animals, microorganisms can utilize a huge variety of energy sources. For example, some microbes can eat hydrogen sulfide, which is highly toxic to most other organisms (including humans), while other microbes can live completely without oxygen by breathing alternative substances such as nitrate, sulfate, iron and even CO2.

This diverse metabolic activity of microorganisms has been intensely influencing Earth's chemistry and climate over billions of years. Even today, microorganisms drive the bulk of biochemical processes in virtually every ecosystem, including most of carbon, oxygen and nitrogen cycling in the ocean. Unraveling the factors that determine how microorganisms are distributed in nature and how their distribution affects biochemical processes is of central importance to environmental sciences, industry, and human health. This is a challenging task because there are a myriad of microbial species in the world; even a single tube of seawater can contain millions of microorganisms and thousands of microbial species. While scientists are making great progress towards identifying and charting microbial species in nature, the patterns so far revealed are incredibly complex to interpret; for example, we usually don't know how variations in present species influence the overall biochemical processes performed by these species.

Charting the metabolic type of ocean's microbes
In our latest study published in the journal Science, we sought to shed light on the above questions by investigating microorganisms across the world's oceans. Our primary goal was to examine how geographic location, environmental factors, as well as the "metabolic type" of microorganisms (i.e., what substrates they use and what reactions they perform to gain energy), affect their distribution in the ocean. To that end, we analyzed microbial DNA sequence data from a recent global ocean survey, in combination with oceanographic data (such as temperature, solar irradiance and various chemical concentrations) from the same survey as well as from satellite images.

Because existing techniques for surveying microorganisms tell us which species are present but not what their metabolic types are, we had to create a new tool that would allow us to translate species identity to metabolic type. Our tool, which we called FAPROTAX (for "functional annotation of prokaryotic taxa"), incorporates information from thousands of previously published experiments with known microorganisms and takes into account their evolutionary relationships, to predict the likely metabolic type of less known species. Using this tool, we classified over 30,000 distinct microorganisms from the ocean survey into their metabolic type. For example, we distinguished between organisms that consume methane (a potent greenhouse gas), organisms that eat sulfide (a toxic gas found in some parts of the ocean) and organisms that use light energy for growth through photosynthesis.

The same biochemical function can be performed by many alterative species
One of our first observations was that a myriad of alternative microbial species could be responsible for the same biochemical process, depending on the location and time of the year. For example, across the ocean we found hundreds of photosynthesizing species, and at each location a different subset of those was present at substantial numbers. Ecologists typically call this phenomenon "functional redundancy", meaning that there is a redundancy in the number of species responsible for each biochemical function. Our finding was perplexing, because ocean currents can disperse microorganisms across large distances, so the presence or absence of a species from one location versus the other could not be explained simply by the inability of that species to reach certain locations. Indeed, we observed no trend of increasing species differences over increasing distance, when taking into account environmental factors.

Environmental conditions determine metabolic type, but not species identity
Using statistical methods, we also discovered that environmental variables (such as depth, temperature and oxygen concentration) could strongly predict the distribution of metabolic types. For example, groups capable of fermentation or breathing nitrate are mostly found in deeper, oxygen-depleted regions, which make sense since in these regions fermentation and nitrate respiration can help cope with the lack of oxygen. In contrast, the same environmental variables failed to predict which microbial species were associated with each metabolic type in any given location. Hence, (as of yet unknown) factors other than the environment and limitation of dispersal seem to influence which species get to perform each type of metabolism in each location.

Our findings imply that if we want to understand why some microbial species are found in specific locations of the ocean and not others, one first needs to consider their metabolic characteristics, i.e. which substrates and what chemical reactions they use to gain energy. Reciprocally, it may be possible to predict biochemical processes in the ocean foremost based on environmental conditions, while knowing exactly which microbial species are present where and when may only be of secondary importance. In particular, major variations in species composition, as frequently observed in the ocean and in other environments, need not necessarily lead to major changes in the overall biochemistry of a system.

Accounting for the metabolic type of microorganisms in environmental surveys can greatly simplify our interpretation of why some species are found in some places and not in others. A metabolism-centric description of microorganisms in mathematical models for ecosystems could also greatly improve our predictions of Earth’s nutrient cycles and climate.

Full scientific article:
Louca, S., Parfrey, L. W., Doebeli, M. (2016). Decoupling function and taxonomy in the global ocean microbiome. Science 353:1272-1277
microbial diversity in a tube of seawater

locations of the Tara oceans survey

grouping microorganisms by metabolic type

taxa-function associations in marine microbes

species composition per metabolic function

Louca lab. Department of Biology, University of Oregon, Eugene, USA
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