Under the microscope, scientists identified SAR11 zombie cells by their distinct lack of ribosomes. In an example comparing a live, infected SAR11 cell to an infected zombie cell: blue indicates bacterial DNA, yellow shows ribosomes, and purple highlights phage genes. The live cell (upper pictures) displays all three colors, while the zombie cell (lower pictures) lacks the yellow ribosome signal. The final column of images on the right merges these colors, clearly distinguishing the two cell types.
© Jan Brüwer/Max Planck Institute for Marine Microbiology.
Aficionados of creationism’s malevolent designer will be interested to learn that researchers at the Max Planck Institute for Marine Biology in Bremen, Germany, have discovered a virus that seriously reduces the population of a marine microbe that is an essential part of the marine food cycle, so seriously depleting the food chain for other marine organisms.
The microbe is a bacterium, know to science as a Pelagibacterale or SAR11, and, as an added piece of nastiness, the virus doesn't just infect the bacterium, it turns it into something that is halfway between dead and alive. In other words, it keeps the essential processes working while it uses the parts it needs to make more copies of itself from the bacterium's mitochondrial DNA.
What are SAR11 microbes and what part do they play in the marine food cycle? SAR11 (short for "Sargasso Sea isolate number 11") are a group of extremely small and abundant marine bacteria belonging to the Alphaproteobacteria class. These microbes are one of the most prolific organisms in the ocean, playing a critical role in the marine ecosystem. Here is an overview of their characteristics and their role in the marine food cycle:The researchers have shown that 20% of the bacteria are infected by the virus and during time when the bacteria are blooming, the virus can reduce their numbers by about 90% in a little as 5 days.
Characteristics of SAR11 Microbes
Role in the Marine Food Cycle
- Abundance: SAR11 are among the most abundant organisms in the ocean, making up about 25% of all microbial plankton cells in the ocean's surface waters. Their populations can reach up to 10^5 to 10^6 cells per milliliter of seawater.
- Size: They are extremely small, typically about 0.2 to 0.3 micrometers in diameter. Their small size and streamlined genomes are adaptations that allow them to thrive in nutrient poor environments.
- Metabolism: SAR11 bacteria are oligotrophic, meaning they are adapted to environments with low nutrient concentrations. They primarily utilize dissolved organic carbon, including simple compounds like amino acids, organic acids, and one-carbon compounds like methanol.
- Genomics: The genome of SAR11 is compact and efficient, with a minimal number of genes necessary for survival and reproduction in the oceanic environment.
SAR11 bacteria play a crucial role in the marine carbon cycle and, by extension, the broader marine food web. Here’s how:Summary
- Carbon Cycling: SAR11 contributes significantly to the carbon cycle by breaking down dissolved organic carbon (DOC) into carbon dioxide through respiration. This process releases carbon dioxide back into the ocean, where it can be used by other organisms, such as phytoplankton, for photosynthesis.
- Nutrient Recycling: By decomposing organic matter, SAR11 helps recycle nutrients, making them available for other microorganisms and higher trophic levels in the food web.
- Base of the Food Web: Although SAR11 itself is not a primary producer, it facilitates the growth of primary producers (such as phytoplankton) by regenerating nutrients. Phytoplankton, in turn, form the base of the marine food web, supporting a variety of marine life from zooplankton to large marine mammals.
- Symbiotic Relationships: SAR11 can form symbiotic relationships with other marine organisms. For example, they might live in close association with phytoplankton, benefiting from the organic matter these primary producers release while providing them with recycled nutrients.
- Global Impact: Due to their sheer abundance and metabolic activity, SAR11 has a significant impact on global biogeochemical cycles, including the cycling of carbon and nutrients. Their activity influences the ocean’s role as a carbon sink and helps regulate the Earth’s climate.
SAR11 microbes are tiny but mighty players in the ocean, crucial for the breakdown of organic matter and the cycling of carbon and nutrients. Their activities support the marine food web and have broader implications for global carbon cycling and climate regulation. Their efficiency and abundance make them key components in maintaining the health and stability of marine ecosystems.
The research has just been published in the journal Nature Communications and is described in a Max Planck Institute news release:
Zombie cells in the sea: Viruses keep the most common marine bacteria in checkTechnical details are in the team's open access paper in Nature Communications:
Marine microbes control the flux of matter and energy essential for life in the oceans. Among them, the bacterial group SAR11 accounts for about a third of all the bacteria found in surface ocean waters. A study by researchers from the Max Planck Institute for Marine Microbiology in Bremen, Germany, now reveals that at times nearly 20% of SAR11 cells are infected by viruses, significantly reducing total cell numbers. The viruses can also transform these once thriving bacteria into zombies, a phenomenon observed for the first time and widespread in the oceans.
The ocean waters surrounding the German island of Helgo-land provide an ideal setting to study spring algae blooms, a focus of research at the Max Planck Institute for Marine Microbiology since 2009. In a previous study, the Max Planck scientists observed a group of bacteria called SAR11 to grow particularly fast during these blooms. However, despite their high growth rates, the abundance of SAR11 decreased by roughly 90% over five days. This suggested that the cells were quickly decimated by predators and/or viral infections. Now, the Max Planck researchers investigated what exactly lies behind 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, lead author
Max Planck Institute for Marine Microbiology, Bremen, Germany.
How does phage infection work? Phages infect bacteria by introducing their genetic material into them. Once there, it replicates, and utilizes the bacterial ribosomes to produce the proteins it needs. Researchers from Bremen used a technology that enabled them to “follow” the phage’s genetic material inside the cell.
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.
Jan Brüwer
While this might seem straightforward, the low brightness and small size of the phage genes made it challenging for researchers to detect them. Nonetheless, thousands of microscope images were successfully analyzed, bringing 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
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
Zombie cells: A global phenomenon
To the surprise of the scientists, the images revealed even more.
Zombie cells represent a novel phenomenon observed not only in pure SAR11 cultures but also in samples collected off Helgoland. Furthermore, analysis of samples from the Atlantic, Southern Ocean, and Pacific Ocean revealed the presence of zombie cells, indicating this phenomenon occurs worldwide.
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.
Jan Brüwer
Brüwer and his colleagues hypothesize that not only SAR11 bacteria, but also other bacteria, can be turned into zombies. Thus, they want to further investigate the distribution of zombie cells and their role in the viral infection cycle.
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.
Jan Brüwer
Abstract
Phages play an essential role in controlling bacterial populations. Those infecting Pelagibacterales (SAR11), the dominant bacteria in surface oceans, have been studied in silico and by cultivation attempts. However, little is known about the quantity of phage-infected cells in the environment. Using fluorescence in situ hybridization techniques, we here show pelagiphage-infected SAR11 cells across multiple global ecosystems and present evidence for tight community control of pelagiphages on the SAR11 hosts in a case study. Up to 19% of SAR11 cells were phage-infected during a phytoplankton bloom, coinciding with a ~90% reduction in SAR11 cell abundance within 5 days. Frequently, a fraction of the infected SAR11 cells were devoid of detectable ribosomes, which appear to be a yet undescribed possible stage during pelagiphage infection. We dubbed such cells zombies and propose, among other possible explanations, a mechanism in which ribosomal RNA is used as a resource for the synthesis of new phage genomes. On a global scale, we detected phage-infected SAR11 and zombie cells in the Atlantic, Pacific, and Southern Oceans. Our findings illuminate the important impact of pelagiphages on SAR11 populations and unveil the presence of ribosome-deprived zombie cells as part of the infection cycle.
Introduction
Pelagibacterales, known as the SAR11 clade, are small free-living marine bacteria that account for 20–50% of planktonic cells in the oceans and are crucial components of marine biogeochemical cycles1. The reasons for their ecological success in the pelagic ocean are still being elucidated1. One proposed explanation was that SAR11 are slow-growing defense specialists, minimally affected by phage predation2. However, several phages infecting SAR11 (pelagiphages) have been described3,4,5,6,7 and studied through cultivation and sequencing efforts with increasing attention in recent years. Metagenomic and -viromic studies not only explored the functional abilities of their genomes8 but also suggest that pelagiphages, including uncultivated representatives, are the most abundant phages in the ocean3,9,10,11,12. Despite the ubiquity of pelagiphages, they appear to have low lytic activity within the host population13,14. However, direct quantifications of pelagiphage infected cells, and thus investigations of their role in controlling SAR11 abundance, have not been done so far.
In a recent study, we identified a contrary trend of cell division rates and cell abundances of SAR11 during the 2020 phytoplankton spring bloom at Helgoland Roads, German Bight15. Phytoplankton spring blooms are characterized by high phytoplankton-derived organic matter availability and a recurring succession of fast-growing specialized bacterial taxa16. Due to low abundances during phytoplankton blooms, SAR11 was generally considered to be outcompeted by specialized taxa. However, when growth rates of SAR11 were measured during the 2020 phytoplankton bloom, SAR11 grew at ~1.9 divisions d−1, while cell abundances decreased by ~90% over 5 days15. As this decrease was specific to SAR11 (compared to other abundant bacterioplankton), we hypothesized viral-induced mortality to cause the discrepancy15. Here, we quantified the number of pelagiphage-infected cells using advanced microscopy techniques. We first established the protocol on pure cultures of the pelagiphages and their hosts and subsequently assessed infection dynamics throughout the phytoplankton spring bloom described above. For a global perspective, we analyzed the distribution of pelagiphage-infected SAR11 cells in cruise samples across the Pacific, Atlantic, and Southern Ocean. Our investigation of the pure cultures and environmental samples has led us to discover ribosome-deprived but phage-infected cells, a new phenomenon during phage infection.Fig. 1: Infection cycle of HTCC1062 infected with HTVC027P and HTVC031P and example epifluorescence microscopy images.
Bargraphs show triplicate samples during the infection cycle. “p.i.” stands for post infection. The negative control was uninfected. Abundance of 100% corresponds to total cell counts of DAPI-stained cells. Example microscopy images on the right display DAPI (DNA; cyan), FISH for 16S rRNA (yellow), and phage genes via direct-geneFISH (magenta). Outlines were drawn manually. Images were recorded using SR-SIM on a ZEISS LSM780 equipped with ELYRA PS.1 and analyzed using the ZEN software. Scale bar: 0.5 µm.
Brüwer, J.D., Sidhu, C., Zhao, Y. et al.
Globally occurring pelagiphage infections create ribosome-deprived cells. Nat Commun 15, 3715 (2024). https://doi.org/10.1038/s41467-024-48172-w
Copyright: © 2024 The authors.
Published by Springer Nature Ltd. Open access.
Reprinted under a Creative Commons Attribution 4.0 International license (CC BY 4.0)
I wonder if I can tempt a creationist to explain these viruses in terms of the design of an omnibenevolent designer who created the world and everything in it for the benefit of human beings, and why they can't be explained as the result of evolution by natural selection working without a plan and with no objective in mind.
Or will we have the traditional response of either pretending not to have seen the challenge or pretending to be too stupid to understand it?
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