Meet the Winners of the 2022 Best Article Award From FEMS Microbiology Ecology

20-02-23 Joseph Shuttleworth

Francesca Vulcano, C.J. Hahn, Desiree Roerdink, Hakon Dahle, Eoghan Reeves, G. Wegener, Ida Steen and Runar Stokke, wrote the excellent research article “Phylogenetic and functional diverse ANME-1 thrive in Arctic hydrothermal vents” for our journal FEMS Microbiology Ecology. This was picked by the FEMS Microbiology Ecology Editors-in-Chief and Section Editors as the best article for 2022. 

We interviewed all the authors to find out more about the inspiration behind this paper:

 

Could you provide a brief, simple overview of the topic your paper covers?

Unlike other archaeal anaerobic methane oxidizers, ANME-1 have a limited metabolism. Nonetheless, ANME-1 have been observed in thermally diverse marine environments, such as cold seeps and high temperatures hydrothermal vents, suggesting a certain physiological flexibility.

We hypothesized that the genetic features underlying this flexibility could be identified by comparing the functions encoded in ANME-1 genomes recovered from thermally diverse environments. By using phylogenomics, we also sought to describe the phylogenetic relationship between ANME-1 from thermally diverse environments to identify lineages with different temperature specificity. ANME-1 genomes were reconstructed from hydrothermal vents along the Arctic Mid Ocean Ridge.

We identified two distantly related ANME-1 phylotypes, indicating that genomes recovered from the same geographical area are not necessarily phylogenetically close. These lineages seemingly preferred opposite thermal regimes, suggesting that temperature can drive ANME-1 distribution. Closely related genomes were often reconstructed from geographically distant areas, indicating that ANME-1 can disperse globally.

Most ANME-1 from hydrothermal vents occupied a basal position within the order suggesting a hydrothermal origin of ANME-1. We observed that recently evolved ANME-1 recovered from Arctic low-temperature hydrothermal sediments and cold seeps worldwide were enriched in genes for defense and survival mechanisms. Hence, cold-adapted ANME-1 might be more resilient than their high-temperature adapted relatives. An evolution towards an increased physiological complexity might have favored the migration of ANME-1 from hydrothermal vents to colder environments.

How was your experience extracting samples from the Arctic Mid Ocean Ridge?

The discovery of hydrothermal vents has revolutionized our understanding of life and its interaction with the environment. Due to their remoteness, hydrothermal vents are still enigmatic environments, and every expedition is a source of awe and excitement and an opportunity to make serendipitous observations. Despite the excitement of exploring the ocean and the remote regions of Earth, sampling hydrothermal vents for ecological studies is challenging and requires careful organization.

The experience with extracting samples from the Arctic Mid Ocean Ridge showed that successful sampling is only achievable by planning several steps ahead and depends on the collaborative effort of several people with different skills. Crucial to our research are the pilots of the remotely operated underwater vehicle and the vessel crew. A good sampling outcome can be achieved by preliminary collection of extensive geochemical and physical metadata preferably combined with long-term observations of geological and biological dynamics via the deployment in situ observatories.

Overall, it is up to the researchers to identify which questions can be answered with the methods and technologies available at the time of the expedition. Metagenomics is currently one of the most efficient approaches for the study of uncultivable lineages. The collection of metagenomic dataset from marine hydrothermal vents is relatively simple and samples can be easily and safely preserved for sequencing. Hence, we opted for a metagenomic-based approach. Our results could be further expanded with additional meta-omics datasets, but the sampling strategy should be optimized to safely recover proteins and mRNA.

What encouraged you to perform research in this area of microbiology?

ANME-1 have a predominant role in removing methane in anoxic marine niches and are crucial for minimizing its warming effect on Earth’s atmosphere. They have already been acknowledged as partially accountable for global-scale climatic changes throughout Earth’s history. Nonetheless, due to their syntrophic lifestyle and the low energy yield of their metabolism, studying their physiology through cultivation has been slow and difficult. Research about physiological traits other than their metabolism has been limited. Understanding the physiological traits at the basis of ANME-1 adaptability is pivotal for predicting how they can respond to or determine climate changes. Their ability to be resilient to environmental stressors, adaptable to temperature changes, and resistant to pathogens might directly affect the integrity of Earth’s biogeochemical equilibrium. These critical aspects primarily motivated our interest in identifying potential adaptation strategies of ANME-1.

Furthermore, we investigated the phylogenetic relationship between genomes from geographically distant sites to ponder the capacity of ANME-1 to reach new anoxic environments and efficiently colonize them. The ability of ANME-1 to disperse relatively freely in oxygenated environments in a dormant state could represent a valuable natural buffering system to counteract, for example, the gradual exposure of hitherto buried methane reservoirs.

What do you see as the next steps in this area of research?

There are several approaches that can contribute to complete and deepen the observations reported in our study. Primarily, efforts should be focused on developing novel enrichment cultures to prove hypothesis on adaptation mechanisms and temperature specificity of ANME-1 lineages. Besides, the comparison of metagenomic datasets worldwide can be used to trace the distribution of ANME-1 species across geographical transects to better study global dispersal patterns. The collection of metagenomic data from new anoxic marine and terrestrial environments can also expand the collection of ANME-1 genomes and potentially reveal a so-far overlooked metabolic versatility.

Thanks to the recent advances achieved by using genome-based phylogenies, studies describing the metabolic evolution of critical microbial taxa are multiplying. It could be interesting in the future to deepen our knowledge on the evolutionary history of ANME-1 and to model how their evolutionary dynamics over a large-scale time frame have intertwined with Earth’s climatic changes.

Finally, metagenomics has recently allowed the identification of overlooked genetic traits of ANME-1. Vestigial hydrogenases have been identified, as well as an extensive ANME-1 virome that likely influences ANME-1 evolution and ecology. It is therefore likely that several other unknown physiological features will be discovered in the years to come by using the magnifying lens of metagenomics and analyzing metagenomic data in depth.

Read the 2022 award winning paper: Phylogenetic and functional diverse ANME-1 thrive in Arctic hydrothermal vents

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