The language of sociomicrobiology: report from a meeting for the Forum on Microbial Threats

Last night I got back from an excellent small meeting at the Institute of Medicine‘s Forum on Microbial Threats. You may wonder what on earth I was doing there, but the actual topic of this workshop was The Social Biology of Microbial Communities, so that makes sense. The chair was David Relman, who did a great job stimulating discussion. I loved the way he always looked so interested and delighted with how things were going. The meeting was tweeted by Jonathan Eisen, @phylogenomics, who did a great job (except for  misspelling my last name).

The meeting was a lot of fun, with great talks, interesting discussion, both formal and informal, and a diversity of people that stretched me in new directions. I could talk about how great small meetings are, what exactly I learned, or how to give a talk to a diverse audience, but for now, I’ll concentrate on language.

We work with microbes, which means we do not need to worry about things like consciousness, theory of mind, or intentionality. But, as one member of the audience kept pointing out, maybe we do need to worry about over-humanizing our microbes and what they do. Microbes may be small, but this does not mean they behave like tiny children on their playground, fighting, cooperating, stealing each other’s cookies, and teaming up to bully the weak or the new.

Or does it? What do we really know about how microbes live?  This is a huge topic, one I can’t possibly cover here, but what I can do is point towards some of the issues. Let’s begin with the title of the meeting and the words it contains, working from the most general down.

What is a community? I would define community as the set of organisms in a shared place and time, where shared is on their scale. Communities are made up of single-species populations, though they can be interwoven into multiple-species organisms (another topic). The individuals in a population need some possibility of interacting, or encountering each other. If individuals have no chance of encountering or competing with each other, they are not of the same population. A mouse in China is not in the same population as a mouse in Texas.

A skeptic would say you have to know a lot to even know where the boundaries of populations or communities are. To know how a population of dragonflies is defined, you would have to know how far they fly, whom they interact with, and what resources concentrate them. And this is before we even begin to discuss migratory species. Ultimately, there will be probabilistic and overlapping boundaries to populations and the communities they populate. But we don’t usually need to worry too much about this. When I studied wasps on the Maracay campus of the Central University of Venezuela, I assumed they were all part of the same population, close enough to interbreed, or plunder the same resources. The community would include all those wasps and everything else living in the area.

So, what is a microbial community? To answer this, we first have to define microbe. I use the most general definition, based on size. Hmm, this is hard. Bacteria and archea are certainly microbes. So are all protists, that vague group that is not phylogenetically based, simply including all single-celled eukaryotes, maybe excluding fungi. Yeast is another non-phylogenetic term that simply means single-celled fungi, though a certain couple of species have hogged the term for themselves. I would throw in viruses, also, for they are small. For the record, in my book they are certainly living, a discussion for another place. We could limit microbes to exclude multicellular organisms, but that may be difficult, since multicellularity pops up fairly easily. Dave Queller and I have worked hard on defining organismality, another topic for another time. Maybe many fungi could be considered microbial, with their tiny hyphae threading through so many environments. You get the idea.

Now we have two words from the title, so we can try putting them together: microbial community. What does this mean? Working from the definitions, we could say it simply means all the small forms of life occurring in the same place and time, where same implies a shared place, with some possiblity they will encounter each other, or take resources the other might have used. The same microbial community may be very much smaller than the community elephants live in, though I’m about to tangle myself up here, since there are also microbes in the elephant community. Furthermore, if microbes blow around, there is some chance they are in huge communities, though we could exclude the world-wide community in favor of a gram of soil based on probabilities of interacting, or competing for the same resources.

One key point is that all microbes are in communities. If they are of a single species, they are in a population. Community and population are not words that say anything about how individuals interact. They simply say that there is a possiblity that they could interact, they could use the same resources. In a way this should be extremely obvious, for all of life is in communities.

One reason we may have a hard time remembering that all microbes are in communities comes from our early focus on microbes that cause disease.  Every microbiologist, including even me, knows and respects Koch’s postulates. What these postulates do is clearly define when we can say a certain organism causes disease (no, I won’t define disease today) in another. To do this, we need to take the microbe out of its community, so we can say this, and no other, caused the disease. The postulates are: that the microbe must be found in individuals suffering the disease, that it can be grown in pure culture, that it can cause disease when added to a new individual, and then that the process can be reiterated, isolated from the new individual and shown to be the same as the original isolate. These postulates are still powerful, but they do not define the way microbes live. They live in multi-species communities.

Yikes! This is getting long, and we haven’t even reached the really cool stuff, the first words of the title.  I’ll keep them together, in the interests of time, yours and mine. Anyway, social biology could just as well have been called sociobiology, like the title of this blog. Social biology focuses on the interactions that being in the same community make possible. It is usually used for within-species interactions, so I’ll cover those first, then extend it to between-species interactions. Social biology is usually used for cooperative or altruistic interactions, not for all interactions, though some argue, and I tend to agree, that there is no conceptual reason for this. The theory of inclusive fitness is what we use to understand what individuals do to increase their genetic representation in the next generation. The subset of the theory called kin selection can be used to predict when individuals will help relatives reproduce at a cost to their own personal reproduction. W. D. Hamilton originated these powerful theories that define our understanding of social interactions. (You may be aware of the recent paper by Nowak et al. on this topic, and the hundreds of responses. This is a human story of power and obfuscation, not a scientific one.)

I’m afraid the hard-written paragraph above may not be that clear to many. What is the bottom line for microbes? I’ve said all microbes live in communities. Does it then follow that all microbes are social? Not necessarily. If there existed a microbe that moved through the soil as a single cell, propelled, perhaps, by a single flagellum, taking in nutrients as it encountered them, then dividing when it got big enough, I suppose you could call it solitary, not social. But if it bumped into another cell and exchanged some genetic material, that would be the social act we could call a form of sex. If it sensed the presence of others through secretions that made it change its trajectory, that would also be a social act.  If it coordinated with others to move in swarms, that would be social. In short, I think it is safe to say, that all microbes are social. This does not mean they all do the same social things. So it is probably most useful when talking about social microbes to define which kinds of social behavior you are considering. Sociomicrobiology is a field that focuses on those behaviors. It is an important field. Perhaps most crucial is that microbiologists not reinvent the wheel, so to speak, but learn from decades of work on social organisms and inclusive fitness theory. This workshop was a great start, but a lot more can be done. A lot of the theory is very counter-intuitive. Its best explainers include Steve Frank, David Queller, Stuart West, Mary Jane West Eberhard and Andrew Bourke.

Here’s one example of within-species cooperation that shows why I’m such a believer that all microbes are social: bacteriocins in bacteria (probably also in archaea).  These toxins kill others of the same species, sometimes with the death of the producer. They benefit close relatives that occur nearby by eliminating competitors, even freeing the nutrients in competitor’s bodies for consumption. Close relatives are immune to the toxins because they have the antidote. Dying to help others is a social act explained by kin selection. Both the toxins and the antidotes have been shown in some systems to be expensive to produce, so they would be lost if not for the fitness gain through kin selection. Check out Ben Kerr’s work on this topic.   There’s tons more I could say, but now maybe is the time to go to the real literature, reviews by my group, West, Travisano, Velicer, Crespi, Griffin, and others.

Between species interactions are not usually called social. They can be divided into harmful, as in predator-prey interactions, or helpful, as in mutualisms. They are generally easier to understand from a social evolution perspective than within-species interactions are, because each partner must benefit directly. Joel Sachs and his group wrote a great review on mutualisms. Specialization, compartmentalization, adopting other organisms for certain tasks, as ants adopt aphids, or mitochondria got adopted by their host, are great leaps in evolution. These are all examples of between-species cooperation, or mutualism. Just be sure to remember, no organism evolves for the exclusive good of another under this evolutionary view of life, or any view of life subject to test.

In sum, the final answer about our language is that we should pay a lot of attention to what goes on in the playground of life, for microbes live in communities, engage in social interactions, and cooperate in ways that can hurt us. If they are all social, then we need to define each time the kind of sociality we are addressing, just as we need to define the other apparently human words like cooperate, cheat, altruism, relative, mutualism, and even kill, hurt, and infect. Science advances best when we understand each other.

Panel discussion after talks.

Jo Handelsman, one of the leaders in the field.

Jonathan Eisen, Forum on Microbial Threats member

 

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About Joan E. Strassmann

Evolutionary biologist, studies social behavior in insects & microbes, interested in education, travel, birds, tropics, nature, food; biology professor at Washington University in St. Louis
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