Rocks and their microbes: a co-evolutionary partnership

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Miles beneath our feet, Earth’s rocky crust may seem a cold, dead place. On closer inspection it’s anything but.

Microbes have been making a home on and in rocks since…well, since the beginnings of life, some 3.5 billion years ago. The traditional view of rock-dwelling microbes is one of sparse, energy-starved survivalists eking out an existence on a hostile frontier. These critters are at the mercy of their environments, their numbers dictated by physical factors – things like temperature and pH.

Geobacter, a rock-dwelling bacteria coating iron oxide minerals. Credit: Wikipedia

Geobacter, a rock-dwelling bacteria coating iron oxide minerals. Credit: Eye of Science

A study published in Geomicrobiology Journal, led by graduate student Aaron Jones at the University of Texas at Austin, challenges the assumption that subsurface microbes are passive survivalists. In a series of lab experiments, Jones demonstrates that mineral-dwelling microbial communities are uniquely adapted to their environments on the scale of individual mineral grains. Moreover, his research suggests microbes and minerals share a partnership that stretches back through geologic time.

Jones was interested in how mineralogy- the composition of the minerals that form rocks- influences the abundance and diversity of microbes. In particular, he was interested in sulfur oxidizers- bacteria that strip electrons from sulfur to acquire energy. Sulfur oxidizers are common in other subsurface environments including deep ocean vents. Their metabolism generates strong acids that eat away at certain minerals, forming cracks, pores, even caves.

In the lab, Jones set up a series of “bioreactors”- tanks in which liquid of a specific chemical composition flows over thin sheets of rock. He used a range of rocks that differ in their mineralogy. These included several rocks composed of calcium carbonate (limestone, dolostone and calcite) and several made of silica-rich minerals (albite, microcline and quartz). Jones inoculated his bioreactors with samples of a sulfur-metabolizing biofilm collected from a Wyoming cave spring.

Example of a benchtop bioreactor. Bioreactors are commonly used in microbial biotechnology for cell culturing and fermentation. Credit: Wikimedia Commons

Example of a benchtop bioreactor. Bioreactors are commonly used in microbial biotechnology for cell culturing and fermentation. Credit: Wikimedia Commons

After three weeks of incubation, he measured bacterial growth, extracted DNA and used pyrosequencing to examine the composition and diversity of the microbial communities formed on different rock types.

Different rocks, different microbes

Growth patterns differed substantially across the carbonate and silicate rocks. On carbonates, bacteria grew in thick, filamentous biofilms. By contrast, growth was much sparser on silicates, with bacteria either accumulating in small clumps or spreading out individually.

Community composition also differed among different rocks. The bacterial phyla Alphaproteobacteria dominated on most carbonates. Sulfur oxidizers that thrive at near-neutral pH were common, representing 17-45 % of the community.

A different picture emerged on the silicate rocks. Members of the phyla Firmicutes and Actinobacteria- also known as Gram-positive bacteria– were found here. While community composition was relatively similar among the carbonates, communities that grew on quartz were very different than those found on albite or microcline. Jones observed fewer sulfur oxidizers on silicates, and those he found tended to be more acid-tolerant.

Composition of bacterial communities grown on different mineral surfaces. From Jones & Bennet 2014.

Composition of bacterial communities grown on different mineral surfaces. From Jones & Bennet 2014.

Perhaps the most obvious conclusion here is that microbes do not select rocks at random. Different growth patterns among rocks tell us this. Better microbial growth on carbonates probably reflects a higher density of essential nutrients, particularly phosphorus. Moreover, two of the silicate rocks, albite and microcline, contain high concentrations of aluminum, a toxic element that restricts bacterial growth.

More subtly, however, there appears to be “selective relationship” between mineralogy and microbial ecology. In other words, the microbes making a living on any given rock are uniquely adapted to taking advantage of, or protecting themselves from, the specific chemical properties of that rock.

This relationship bears itself out in many ways. For one Jones found more acid-tolerant microbial communities on silicate rocks. Remember, acid is a byproduct of sulfur metabolism. Carbonate rocks have a high “buffering capacity”, meaning their minerals react with and neutralize acid. By contrast, silicate rocks, especially quartz, are pretty unreactive. Rather than eating away at minerals, acid accumulates at silicate surfaces. The presence of acid-loving bacteria on quartz suggests a feedback loop between sulfur metabolism, mineralogy and microbial community structure.

The presence of Gram-positive bacteria on silicates also underscores the relationship between microbial community composition and the mineral environment. The cell walls of Gram-positives possess unique chemical properties that promote bonding with silicate surfaces. This microbe-mineral binding, known as adhesion, is a key element of survival for most rock-dwelling bacteria. By adhering to a solid surface, bacteria can mine nutrients and form protective biofilms.

Even microbes living on the undesirable aluminum-rich rocks may possess unique adaptations. While few bacteria grew on albite or microcline, these sparse populations were highly diverse. The unique challenges presented by a toxic environment may serve to maintain competition, preventing any single group of organisms from gaining dominance.

Our planet’s rocky subsurface is the largest microbial habitat, but we still know very little about its inhabitants. Most microbial ecologists prefer to study environments they can see, feel and intimately relate to. Jones’s research points to complex ecological interactions between microbes and minerals in the deep, dark depths of the world. Rocks shape microbial communities, but microbes may also shape rocks in profound ways. This study lends evidence to a deep synergy between the geological and biological evolution of our planet.

ResearchBlogging.org

Jones, A., & Bennett, P. (2014). Mineral Microniches Control the Diversity of Subsurface Microbial Populations Geomicrobiology Journal, 31 (3), 246-261 DOI: 10.1080/01490451.2013.809174

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When infection is a good thing: sulfur-eating bacteria enlist viruses to help acquire energy

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“Black smokers”, deep sea vents where hot, sulfur-rich fluids bubble up from beneath the ocean floor, are considered hotspots of microbial activity. They may even be where life originated. Credit: Wikimedia Commons

Life is no cake walk at the ocean floor, where carbon is scarce and light nonexistent.  At least near deep ocean vents, mineral-rich water bubbles up from magma beneath the crust, providing both heat and a source of energy. In these alien environments, lithotrophs– bacteria that eat minerals instead of organic carbon- have staked out a niche by evolving some creative metabolic strategies.

But minerals are a poor source of energy compared to organic matter. Lithotrophs are slow-growing critters, easily outcompeted when carbon is abundant. They need all the help they can get. And it turns out, they might very well get help… from an unlikely source. A study published last week in Science Express reports how viruses may be helping deep marine bacteria eat sulfur.

Viruses are everywhere- in soils, skies, oceans, plants and animals, even deep beneath the ocean floor.  In spite of their ubiquity, it’s not well-known how viruses influence marine bacteria and the nutrient cycles they drive.

To study the impact of viruses on sulfur-eating bacteria, a team of scientists led by Dr. Karthik Anatharaman at the University of Michigan collected samples from five different hydrothermal vents : four in the Western Pacific Ocean and one in the Gulf of California. They used shotgun metagenomic sequencing to look at the genomes of the bacteria and viruses present in these environments.

The researchers found five different virus “types” that carried two genes involved in sulfur metabolism. Known as rdsrA and  rdsrC, these genes encode different pieces of dissimilatory sulfite reductase, an enzyme that breaks down elemental sulfur.

How and why did viruses come to acquire these genes? Not technically considered alive, viruses don’t really need enzymes because they don’t perform metabolism on their own. A virus’s sole purpose is to infect a host with its genetic code so that it can turn the host cell into a virus factory. But during viral replication, pieces of  DNA can be accidentally snipped out of the host and integrated into the viral genome. The scientists found bacteria in the same samples carrying both the rdsrA and rdsrC genes. It’s likely that accidental incorporation of host DNA is how viruses ended up with sulfur genes in the first place.

While acquiring sulfur genes may have been a complete accident, viruses appear to have been actively maintaining those genes for a long time.

When the scientists compared rdsrA and rdsrC from viral and bacterial genomes, they found something interesting: completely different DNA sequences surrounding the genes. If viruses had acquired sulfur genes during recent replication errors, some of the nearby DNA would probably have come along for the ride as well. That completely different DNA sequences surround the sulfur metabolism genes in bacteria and viruses suggests viruses have been passing along rdsr genes, generation to generation, for a very long time. In other words, sulfur metabolism genes are being maintained  in viruses by natural selection.

Why would deep sea viruses bother to maintain sulfur metabolism genes they don’t use?  It turns out these viruses may actually have a use for sulfur genes, albeit an indirect one: helping out their hosts. By carrying genes that bacteria can make use of, viruses may assist their hosts in acquiring energy. The ability of sulfur-eating bacteria to acquire energy is ultimately limited by how quickly they can decode their sulfur genes to build enzymes that can do the work. But if a bacteria were to contain viruses with extra copies of the genes it needs, that could help speed the process along. In essence, when a sulfur virus infects a sulfur bacteria, it donates genes that its host can use.

What’s a virus to gain from all of this? Remember, a virus’s sole purpose is replication. Staying in your host’s good graces has its perks. An “infected” bacteria that can acquire energy faster than its neighbors may be able to grow and reproduce faster- leading to more infected offspring, and more viruses. By supplementing host metabolism, viruses may help ensure their continued survival.

This study sheds light on a potentially widespread, mutually beneficial ecological interaction between bacteria and viruses. Lithotrophs in the deep ocean play an important role in the global sulfur cycle and have done so for billions of years. By giving an adaptive advantage to sulfur-eaters and helping them survive, it’s possible viruses have played an equally important role in the geochemical evolution of our planet.

ResearchBlogging.org

Anantharaman, K., Duhaime, M., Breier, J., Wendt, K., Toner, B., & Dick, G. (2014). Sulfur Oxidation Genes in Diverse Deep-Sea Viruses Science DOI: 10.1126/science.1252229