Phages and Zombie Cells Regulate Abundant Marine Bacteria

The movement of matter and energy required for ocean life is regulated by marine microbes, of these, approximately one-third are members of the bacterial group SAR11. These are found in surface ocean waters.

According to a recent study by scientists at the Max Planck Institute for Marine Microbiology in Bremen, Germany, viruses can infect up to 20% of SAR11 cells, significantly lowering the total number of cells. Additionally, the viruses have the ability to turn these once-thriving bacteria into zombies, a phenomenon that has only recently been widely documented in the oceans.

Since 2009, the Max Planck Institute for Marine Microbiology has focused its research on spring algae blooms. The ocean waters surrounding the German island of Holland provide a perfect environment for this study. Scientists at Max Planck discovered in a previous study that a particular strain of bacteria known as SAR11 grew exceptionally quickly during these blooms.

Nonetheless, over the course of five days, the abundance of SAR11 dropped by around 90% despite their rapid growth rates. This implies that predators and/or viral infections swiftly wiped out the cells. The Max Planck researchers have now investigated the precise cause of this phenomenon.

Finding the Phages Infecting SAR11

We wanted to find out if the low numbers of SAR11 were caused by phages, that is viruses that specifically infect bacteria, answering this seemingly simple question was methodologically very challenging.

Jan Brüwer, PhD Student, Department of Molecular Ecology, Max Planck Institute for Marine Microbiology

Bruwer conducted this study as part of his doctoral thesis.

How does infection by phages occur? Phages infect bacteria by introducing their genetic material. Once there, they use the bacterial ribosomes to replicate and produce the proteins they require. Bremen researchers employed a technology that allowed them to “follow” the phage's genetic material inside the cell.

Jan Brüwer explained, “We can stain the specific phage genes and then see them under the microscope. Since we can also stain the genetic material of SAR11, we can simultaneously detect phage-infected SAR11 cells.

Although this may seem obvious, researchers found it difficult to detect the phage genes because of their small size and low brightness. Nevertheless, millions of microscope images were successfully analyzed, and the results included some exciting news.

We saw that SAR11 bacteria are under massive attack by phages, during periods of rapid growth, such as those associated with spring algae blooms, nearly 20% of the cells were infected, which explains the low cell numbers. So, phages are the missing link explaining this mystery."

Jan Brüwer, PhD Student, Department of Molecular Ecology, Max Planck Institute for Marine Microbiology

Zombie Cells: A Global Phenomenon

The scientists were surprised to discover even more in the images.

We discovered that some of the phage-infected SAR11 cells no longer contained ribosomes. These cells are probably in a transitional state between life and death, thus we called them 'zombie' cells."

Jan Brüwer, PhD Student, Department of Molecular Ecology, Max Planck Institute for Marine Microbiology

Zombie cells exhibit a unique phenomenon that has been observed in both pure SAR11 cultures and samples gathered from Iceland. Furthermore, the presence of zombie cells was discovered by analysis of samples from the Atlantic, Pacific, and Southern Oceans, indicating that this phenomenon occurs globally.

Jan Brüwer explained, “In our study, zombie cells make up to 10% of all cells in the sea. The global occurrence of zombie cells broadens our understanding of the viral infection cycle, we suspect that in zombie cells, the nucleic acids contained in the ribosomes are being broken down and recycled to make new phage DNA.”

It is hypothesized by Brüwer and his colleagues that other bacteria, in addition to SAR11 bacteria, can be transformed into zombies. Therefore, they aim to investigate the distribution of zombie cells and their function in the viral infection cycle in more detail.

Brüwer stressed, “This new finding proves that the SAR11 population, despite dividing so fast, is massively controlled and regulated by phages; SAR11 is very important for global biogeo­chemical cycles, including the carbon cycle. Therefore their role in the ocean must be re­defined. Our work highlights the role of phages in the marine ecosystem and the importance of microbial interactions in the ocean.”

Source:
Journal reference:

Brüwer, J. D., et al. (2024) Globally occurring pelagiphage infections create ribosome-deprived cells. Nature Communications. doi.org/10.1038/s41467-024-48172-w

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