Periodic Reporting for period 2 - ASymbEL (A multilevel approach to address the role of Archaeal Symbionts in the Evolution of Life)
Reporting period: 2022-08-01 to 2024-01-31
Microbial symbioses play an essential role in most aspects of life’s evolution. Yet, despite the importance of symbioses, our knowledge is based on a limited number of microbial host-symbiont systems, few of which include Archaea. Considering that Archaea comprise a primary domain of life next to the much better studied Bacteria, and that Archaea engaging in symbiotic interactions are hypothesized to have played a major role in the evolution of complex eukaryotic cells, this represents a severe lack in our understanding of the deep history of cellular life and our own origins.
Notably, recent cultivation-independent approaches have revealed two very diverse microbial groups of archaeal and bacterial symbionts referred to as DPANN and CPR, respectively. These symbionts have small genomes and cell sizes and seem to be obligately dependent on partner organisms for growth and survival. However, the hosts of most of these symbionts are unknown and their effect on host populations in the environment has not been addressed so far. Furthermore, the placement of these lineages in the tree of life is unclear: for example, initial work suggests that they may diverge early from the tree of life raising questions as to whether these organisms could help us to better understand the nature of cellular life in the deep past.
The major aims of ASymbEL are to test the hypotheses that (a) DPANN, together with CPR, have key positions in the tree of life, requiring to revise our view on the early evolution of cells and (b) that the diverse DPANN substantially shape the evolution of life through symbiont-host interactions. To this end, we integrate knowledge from both micro- and macroevolutionary levels and use both computational and experimental approaches. Together, this will shed light on the mysterious DPANN archaeal symbionts and their role in life’s biodiversification.
Notably, recent cultivation-independent approaches have revealed two very diverse microbial groups of archaeal and bacterial symbionts referred to as DPANN and CPR, respectively. These symbionts have small genomes and cell sizes and seem to be obligately dependent on partner organisms for growth and survival. However, the hosts of most of these symbionts are unknown and their effect on host populations in the environment has not been addressed so far. Furthermore, the placement of these lineages in the tree of life is unclear: for example, initial work suggests that they may diverge early from the tree of life raising questions as to whether these organisms could help us to better understand the nature of cellular life in the deep past.
The major aims of ASymbEL are to test the hypotheses that (a) DPANN, together with CPR, have key positions in the tree of life, requiring to revise our view on the early evolution of cells and (b) that the diverse DPANN substantially shape the evolution of life through symbiont-host interactions. To this end, we integrate knowledge from both micro- and macroevolutionary levels and use both computational and experimental approaches. Together, this will shed light on the mysterious DPANN archaeal symbionts and their role in life’s biodiversification.
During the first project period, we have been able to reconstruct a dated tree of life with the most likely root lying between the Archaea and Bacteria. Notably, in contrast to initial expectations, the CPR bacteria do not form a deep branch in this tree. Instead, they form a sister branch of the Chloroflexota – a bacterial lineage that does not consist of symbionts. Together with other recently published work, this indicates that the symbiotic CPR bacteria have evolved from a more complex ancestor that lost genes over time and evolved a symbiotic lifestyle secondarily. On the other hand, while the root of the Archaeal tree remains unresolved so far, our work suggests that the DPANN archaea indeed diversify early in evolution but include lineages that are not genome-reduced and host-dependent. In ongoing efforts, we are now trying to reconstruct how the last common ancestor of all life and of the Archaea looked like and how the various symbiotic archaeal lineages evolved through time.
We are also evolving a DPANN symbiont in the laboratory with its host to study its effect on genome evolution in real time and on at much smaller time scales. Furthermore, we are studying the genomes of archaeal symbiont populations in the environment to assess host-symbiont dynamics and the effect of the symbionts on natural host populations. To this end, we have sampled environments in which these symbionts are abundant over the course of a year and started to establish computational pipelines that provide the basis for the analysis of this data. Finally, we are enriching symbionts in the laboratory with the aim to identify their hosts, establish co-cultures and characterize novel symbiont-host systems that are so far only known from genomic data.
We are also evolving a DPANN symbiont in the laboratory with its host to study its effect on genome evolution in real time and on at much smaller time scales. Furthermore, we are studying the genomes of archaeal symbiont populations in the environment to assess host-symbiont dynamics and the effect of the symbionts on natural host populations. To this end, we have sampled environments in which these symbionts are abundant over the course of a year and started to establish computational pipelines that provide the basis for the analysis of this data. Finally, we are enriching symbionts in the laboratory with the aim to identify their hosts, establish co-cultures and characterize novel symbiont-host systems that are so far only known from genomic data.
With our published and collaborative work, we have been able to contribute to a better understanding of deep cellular evolution by providing evidence for the late evolution of CPR symbionts within the Bacteria in line with a complex bacterial ancestor. We have also been able to contribute improved methods for the study of genome evolution through time and established a new approach for dating this tree of life in the context of geological data. These methodological advances not only led to interesting findings such as the younger age of the Last Archaeal Common Ancestor relative to the Last Bacterial Common Ancestor but will also support prospective analyses of us and the scientific community more broadly. We hope that our ongoing efforts to study not only deep cellular evolution but also the impact of DPANN symbionts on their hosts will provide equally valuable insights and contribute novel methodology in the coming project period. For instance, our initial data suggests that at least one of our DPANN symbionts can lead to the lysis of its host thereby negatively impacting host fitness. In turn, this system provides a promising basis to better understand host-symbiont interactions and the ecological role of these organisms.