Evolutionary oddball has seven genomes inside a single cell

A single-celled alga collected more than 50 years ago and grown in labs ever since has turned out to be a bizarre conglomeration of once-independent organisms, with no fewer than seven different genomes inside it.

“As far as I know, seven is a record number of distinct genomes in a single cell,” says Emma George, who carried out the work while at the University of British Columbia in Canada.

The alga, of a kind called a cryptomonad, was collected by the naturalist Ernst Georg Pringsheim sometime before 1970 and became part of a collection at the University of Goettingen in Germany. In 1988, a microscopic study revealed bacteria within the algal cells, and also viruses within some of the bacteria.

After reading this study, George asked for samples of the alga so her team could sequence all the DNA inside the cells and identify the virus and bacterium within it.

It isn’t that unusual for cells to play host to symbiotic bacteria. Complex cells are thought to have arisen around 3 billion years ago when a bacterium started living inside another simple cell and formed a partnership, a phenomenon known as endosymbiosis. That bacterium evolved into the energy-producing mitochondria found in almost all complex cells.

While the main genome of complex cells is in the cell nucleus, mitochondria still retain their own small genome. This means most animal cells have two distinct genomes, with up to several thousand copies of the mitochondrial genome per cell.

Around a billion years ago, plant cells gained the ability to photosynthesise by acquiring a cyanobacterium. This evolved into the chloroplast, which has also retained part of its genome, so plant cells have three different genomes.

Cryptomonad algae, however, aren’t plant cells. They started out as free-swimming predatory cells and gained the ability to photosynthesise by engulfing a complex plant cell – a red alga – rather than a cyanobacterium.

The nucleus of this red alga has been retained in a shrunken form because it contains some genes essential for photosynthesis. So all cryptomonads have four distinct genomes: the main genome in the cell nucleus, the remnant nucleus of the red alga, the mitochondrion and the red algal chloroplast.

The Goettingen strain has an extra three distinct genomes. It has acquired not just one but two additional bacterial endosymbionts, George’s team found, one of which is infected with a bacteriophage virus.

“For there to be two different ones and then one of them infected with a phage, all within a single cell, it’s amazing,” says George.

Her team identified the host cell as Cryptomonas gyropyrenoidosa, the two bacteria as Grellia numerosa and Megaira polyxenophila, and the virus infecting M. polyxenophila as MAnkyphage.

George thinks this conglomeration existed in the alga collected by Pringsheim and has been passed down to all its descendants ever since, over around 4400 generations.

Surprisingly, the phage-infected bacterium is more abundant in the host cryptomonads than the non-infected bacterium. How the phage has persisted without wiping out its host bacterium isn’t clear, but the phage does have genes that might help the bacterium get along with the cryptomonads, says George. “There must be a balance in that system,” she says.

The study is thoroughly researched, says Dave Speijer at the University of Amsterdam in the Netherlands, who studies the evolution of complex cells, and shows that the relationships between the host and the bacteria and virus within it are surprisingly complex. But he wonders if these relations would survive in real-world conditions or have persisted only because of the stable lab environment the cells have been kept in.

It was already known there are single-celled organisms called dinoflagellates that host single-celled algae called diatoms inside them, with at least six distinct genomes in one cell. One of these “dinotoms” discovered by Norico Yamada at the University of Konstanz in Germany acquired diatoms on four separate occasions and might have nine distinct genomes.

But Yamada says her unpublished results suggest the same diatom species was acquired on each occasion, meaning it might still have only six distinct genomes, depending on what you count as distinct.

“Either way, both systems are extremely complex, and these ‘records’ will likely be beaten by another system yet to be discovered,” says George.