Archaea represent a fundamental life domain that plays a crucial role in the evolution and ecosystem functioning of Earth's biosphere. However, the research history of archaea is relatively brief compared to that of eukaryotes and bacteria. In 1977, Carl Woese and George Fox introduced the concept of "archaebacteria" based on an analysis of the 16S rRNA gene sequence. Subsequently, in 1990, Woese et al. formally designated this group as "archaea". During this period, our understanding of archaea was largely associated with extreme environments, leading to the belief that archaea solely thrived in conditions such as high salinity, elevated temperatures, or oxygen-depleted environments.

In 1992, Jed Fuhrman and Edward DeLong made a breakthrough by identifying two novel types of archaea in marine water. These newly discovered archaea exhibited significant differences from those inhabiting extreme environments. DeLong subsequently coined the terms Marine Archaea I (MGI) and Marine Archaea II (MGII) to categorize these distinct marine archaeal groups. The successful cultivation of the pure MGI culture strain was achieved in 2005. Consequently, substantial advancements were made in comprehending the physiological and ecological roles, as well as the origin and evolution of MGI. However, the cultivation of a pure MGII culture strain has remained elusive up to the present day.

Employing molecular biology, metagenomics, bioinformatics, and other advanced techniques, extensive research has been conducted on the distribution, diversity, and ecological functions of MGII. MGII is now recognized as the most abundant heterotrophic planktonic archaea in the ocean, playing a pivotal role in the global carbon cycle and influencing climate dynamics. Nevertheless, the lack of high-quality genomes has hindered in-depth investigations into the origin and evolutionary history of MGII.

Figure 1. Illustration of the thermal origins of MGII and the distribution of various MGII groups.

Under the leadership of Chair Professor Chuanlun Zhang from the Department of Ocean Science and Engineering at the Southern University of Science and Technology (SUSTech), in collaboration with several domestic and international scientific research institutes, they have recently made significant strides in marine archaeal research. These advancements have unveiled, for the first time, the thermal origin characteristics and potential evolutionary process of marine heterotrophic planktonic archaea MGII.

Their findings, entitled "A Moderately Thermophilic Origin of a Novel Family of Marine Group II Euryarchaeota from the Deep Ocean", have been accepted by the esteemed rapidly growing international journal iScience.

In this study, metagenomic sequencing and bioinformatics analyses were carried out on water samples obtained from various depths within the Mariana Trench's "Challenger" abyss. This investigative approach offered preliminary insights into the thermal origin attributes and possible evolutionary trajectory of MGII. As depicted in Figure 1, the color-coded cells—green, blue, and red—represent MGIIa, MGIIb, and MGIIc, respectively. Their dispersion within seawater manifests as follows: MGIIa predominates in surface seawater, MGIIb primarily occupies subsurface seawater, while MGIIc is predominantly found in deep seawater. Strikingly, all three MGII groups were detected in hydrothermal vent plumes of submarine volcanoes, implying that these submarine hydrothermal vents could be the original habitat of MGII archaea.

Referring to the well-established principle of complementary base pairing—where G (guanine) pairs with C (cytosine), and A (adenine) pairs with T (thymine)—the study underscores the differing strengths of the hydrogen bonds. Bonds between GC pairs consist of triple bonds, demanding higher energy for separation compared to the double bonds within AT pairs. This principle guides DNA replication, indicating that higher GC content generally corresponds to higher annealing temperatures. Based on linear regression analysis between the GC content of the 16S rRNA gene and Optimal Growth Temperature (OGT), the research speculates that MGIIc, MGIIb, and MGIIa present in the ocean exhibit OGTs of 47-50°C, 37°C, and 30-37°C, respectively (as illustrated in Figure 2A).

Drawing upon the linear relationship between GC content and OGT of the 16S rRNA stem sequence, the study infers that the common ancestor of MGII likely had an OGT of approximately 60°C. Furthermore, the OGTs of the ancestors of MGIIc, MGIIb, and MGIIa are estimated to be around 57°C, 49°C, and 46°C, respectively (as depicted in Figures 2B and 2C). The inferred OGT of the MGII ancestor exceeds that of contemporary MGII, suggesting an evolutionary trend of these microorganisms adapting from high to low temperatures.

Enzymatic activity experiments support these findings, revealing that the optimal temperature for the enzymatic activity of β-galactosidase within the MGIIc genome is 50°C—consistent with the OGT estimates derived from GC content (Figures 2D and 2E). Consequently, the research concludes that the prevailing MGIIc's optimum growth temperature in the ocean is approximately 50°C, while its ancestors' optimum growth temperature hovers around 57°C.

The study postulates that MGIIc may have originated from a common ancestor thriving in warm marine environments like hydrothermal vents. Consequently, the researchers have christened this new group as "Candidatus Qianlongarchaea bathyliensis fam. sp. nov".

Figure 2. Illustration of the thermal origin of MGII, substantiated through linear regression analyses correlating the GC content of 16S rRNA genes (A) and stem sequences (B) with optimal growth temperature (OGT). Panel (C) displays the estimated OGT of the common ancestor of MGII as approximately 60°C. Notably, enzyme activity experiments demonstrate that the upper limit for activity temperature of MGIIc is approximately 50°C.

Haodong Liu, Weiwei Liu, and Jose M Haro-Moreno are the co-first authors of this work. Chair Prof. Chuanlun Zhang from SUSTech and Prof. Francisco Rodriguez-Valera from Miguel Hernández University are the co-corresponding authors. The first contributing institution is the Department of Ocean Science and Engineering at SUSTech. ChatGPT was utilized in assisting the editorial need of this article; any generated text has been reviewed and revised for accuracy.

This work was supported by the Hydrosphere Program of the National Natural Science Foundation of China (NSFC) and the Shenzhen Key Laboratory of Marine Archaea Geo-Omics.

Paper link: https://doi.org/10.1016/j.isci.2023.107664

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