Mapping the Landscape of Marine Giant Virus Research: A Scientometric Perspective (1996–2024)

Abstract

Although giant viruses have introduced new perspectives on the definition and evolution of viruses and are increasingly recognized for their significant biological roles within marine ecosystems, systematic evaluations of development trends and scientific contributions in this research field remain limited. This study conducted a bibliometric analysis of the global academic literature on marine giant viruses (MGVs), focusing on nucleocytoplasmic large DNA viruses (NCLDVs), from 1996 to 2024. Using the Web of Science Core Collection, 1544 publications related to giant viruses were identified. After filtering using marine-related keywords and manual review, 300 studies specifically addressing marine giant viruses were selected for the final analysis. This study comprehensively examined the structural characteristics and evolutionary trends in this field by analyzing annual publication productivity, citation patterns, contributions by countries and institutions, author collaboration networks, and keyword co-occurrence patterns. The results show that research on MGVs has steadily increased since the mid-2000s, with a notable surge after 2018 driven by advancements in metagenomics, next-generation sequencing technologies, and global ocean exploration initiatives. The United States and France have taken leading positions in terms of research productivity and impact, with key institutions such as the CNRS (Centre National de la Recherche Scientifique) and Aix-Marseille Université playing central roles. A multipolar network of international collaborations between countries and institutions has been formed. Research topics have evolved from an early focus on virus classification and genome analysis to more diverse themes, including interactions with marine microbiota, viral ecological functions, infection dynamics, virophage research, and metagenome-based ecosystem-level studies. This study provides an overview of the chronological and structural evolution of the marine giant virus research field by systematically presenting key research themes and collaborative networks. The results provide a valuable foundation for determining future academic directions and planning strategic research initiatives. Furthermore, it is expected to facilitate interdisciplinary research in marine biology, environmental science, systems biology, and artificial intelligence-based functional predictions.

1. Introduction

Oceans cover approximately 70% of the Earth’s surface and constitute a vast ecosystem responsible for nearly half the planet’s total biological productivity [1]. Microorganisms are the most abundant life forms in marine ecosystems, with viruses functioning as their primary regulators. Marine viruses infect bacteria and eukaryotic microalgae, lyse their hosts, and facilitate the recycling of organic matter and nutrients through the viral shunt, thereby playing a crucial role in the cycling of carbon and nitrogen [2,3]. Viral infections significantly influence plankton community structures, maintain biodiversity, drive energy flows within marine food webs, and affect microbial evolution [4,5,6]. Among viruses, giant viruses are distinguished by their unique morphological and genetic traits and are particularly significant in their interactions with eukaryotic microorganisms, thereby playing important roles in marine ecosystems [7,8,9].

Marine giant viruses (MGVs), belonging primarily to the phylum Nucleocytoviricota, represent one of the most ecologically significant components of the marine virosphere. Recent metagenomic surveys estimate that MGVs account for a substantial fraction of double-stranded DNA viruses in global oceans, with relative abundances ranging from 5–15% of viral metagenomic reads in surface waters to over 20% in productive coastal zones [10,11]. These viruses are widely distributed across diverse marine habitats, including open oceans, coastal waters, polar seas, and deep-sea ecosystems [11,12]. Representative MGVs include Mimivirus, the first giant virus described with a 1.2 Mb genome infecting Acanthamoeba [13]; Pandoravirus, which possesses the largest known viral genome (>2.5 Mb) [14]; Pithovirus, identified from Siberian permafrost with a ~600 kb genome infecting amoebae [15]; and Megavirus, a close relative of Mimivirus discovered in marine waters with a genome exceeding 1 Mb [16]. Other notable MGVs include Cafeteria roenbergensis virus, a key model infecting marine protists [17], and algal viruses such as Chlorovirus and Tetraselmis virus, which infect green algae and frequently harbor photosynthesis-related auxiliary metabolic genes that link viral infection to primary production processes in marine ecosystems [18,19]. Their sources are linked to infections of a broad range of eukaryotic hosts, such as haptophytes, chlorophytes, prasinophytes, and heterotrophic protists, which serve as key primary producers and microbial grazers in marine food webs [17,20]. Once released into seawater, MGV particles are transported through vertical mixing, ocean currents, and particle-associated sinking, influencing both local and basin-scale viral dispersal [12,21].

Interactions between MGVs and marine biota strongly affect ecosystem functioning. For example, Coccolithovirus infections of Emiliania huxleyi can terminate large-scale algal blooms, thereby regulating carbon export to the deep ocean [22]. Similarly, infections by Pandoravirus and Mimivirus lineages reshape host metabolic pathways by encoding auxiliary metabolic genes, altering nutrient cycling processes in situ [23,24]. The fate of infected cells and viral progeny is also shaped by virophage interactions, grazing pressure, and environmental stressors [25]. Importantly, multiple abiotic factors—including temperature, salinity, nutrient availability, light penetration, and mixing regimes—modulate the abundance and activity of MGVs. For instance, higher sea surface temperatures and nutrient stratification have been linked with shifts in MGV community structure, whereas polar and mesopelagic waters harbor distinct assemblages with unique functional profiles [10,11].

Recent technological advancements in metagenomics, single-cell genomics, and reconstruction of environmental metagenome-assembled genomes have facilitated the discovery of previously undetectable giant viruses in marine environments [10,26]. Genomic data derived from global ocean exploration projects, such as the Tara Oceans, Malaspina, and GO-SHIP, have become essential resources for analyzing the biogeographical distribution, evolutionary lineage, and metabolic functions of various giant virus clades [27,28]. These studies have revealed that MGVs are distributed across a wide range of marine zones, from tropical to polar regions, and exhibit unique community structures that depend on seasonal and vertical stratification in the water column [10,29]. Furthermore, certain giant viruses engage in tripartite interactions with virophages and hosts, shaping coevolutionary trajectories and introducing new dimensions into marine microecology [25,30].

Interest in giant viruses has gradually increased over the past two decades, and academic publications in this area have expanded in tandem with the growing recognition of their ecological and evolutionary significance. However, existing bibliometric analyses have primarily focused on environmental viruses [31], with very few studies specifically targeting MGVs. This study, therefore, aims to identify the research trends and structural patterns in the field of MGVs. This study poses the following questions. (1) How has scholarly research on MGVs changed quantitatively and qualitatively over time? (2) Which countries, institutions, and researchers have played a central role in productivity and impact? (3) What changes in research topics can be observed through keyword frequency and co-occurrence analyses? (4) What structures of international collaboration emerge from the co-authorship network analysis? By addressing these questions, this study provides an objective overview of the structural characteristics and knowledge of ecosystems in MGV research. It offers foundational insights that can support future research directions, policy recommendations, and the strategic planning of international collaborative studies.

2. Materials and Methods

2.1. Data Collection and Selection Criteria

In this study, we conducted a bibliometric analysis of academic publications on MGVs published between 1996 and 2024. The literature data were collected from the Web of Science Core Collection (WoSCC) provided by Clarivate Analytics, a leading citation index database widely used in scientometric research [32,33]. For reliability and scope, only documents included in the Science Citation Index Expanded subset of the WoSCC were analyzed.

A literature search was performed using the major keywords related to giant viruses, including giant virus, NCLDVs, nucleocytoplasmic large DNA virus, Mimivirus, Pandoravirus, pithovirus, Megavirus, Marseillevirus, Faustovirus, Medusavirus, and Mollivirus. These keywords were combined using logical operators (AND, OR) with marine-related terms, such as marine, ocean, sea, coastal, marine environment, and marine microbiome, to focus specifically on studies of giant viruses in marine environments. The search targeted titles, abstracts, author keywords, and Keywords Plus fields, resulting in 1544 large virus-related publications. After manually reviewing the abstracts and full texts, 300 publications closely associated with MGVs and their ecosystems were selected for final analysis. Two independent reviewers assessed the relevance of the documents, and any disagreements were resolved by consensus with a third reviewer [34]. This multistep filtering process ensured a high level of thematic relevance.

2.2. Bibliometric Analysis

A multilayered bibliometric analysis was conducted using various software tools. The bibliometrix package in R (ver. 4.5.1) was used to clean and process the data extracted from the Web of Science and calculate key bibliometric indicators [33]. Keyword co-occurrence and clustering analyses were performed using the VOSviewer (ver. 1.6.20) [35]. Microsoft Excel and Tableau (ver. 2025.2.2) were used for the complementary visualization of time-series statistics, such as annual publication trends and citation changes.

Four main categories of indicators were defined for the analysis. First, publication productivity and scholarly impact were evaluated using metrics such as the number of publications per year, cumulative publications, annual growth rate, and citations per publication [36]. Second, the collaborative intensity between countries and institutions was visualized through co-authorship networks, with centrality measures (e.g., degree centrality and density) used to assess the structure of collaborations [37]. Third, author keywords and Keywords Plus were subjected to co-occurrence analysis to identify research topic clusters and examine the thematic evolution of the field over time [38]. Fourth, the most highly cited publications were identified to extract influential literature within the field, and their citation network structures were analyzed.

As this analysis was limited to the WoSCC database, some relevant studies indexed in other databases such as Scopus, PubMed, and Google Scholar may have been omitted. Additionally, inaccuracies in keywords or abstracts may have led to the exclusion of relevant articles from the search results. These limitations should be considered when interpreting the results [39].

3. Results

3.1. Annual Trends in Publications and Citations

A literature search based on titles, abstracts, and keywords yielded 1544 publications related to giant viruses. Of these, 309 publications were identified as marine-related. After excluding duplicates and irrelevant records, 300 publications were selected for final analysis (Figure S1a). Original research articles were the most prevalent, accounting for 257 publications (85.7%), followed by review articles (34 publications, 11.3%), editorials (three publications, 1.0%), and others (six publications, 2.0%) (Figure S1b).

To investigate the temporal progression of MGV research, publication and citation trends were examined by year (Figure 1). Marine-related publications accounted for approximately 19.4% of all literature on giant viruses. The average annual number of marine MGV publications during the study period (1996–2024) was approximately 10.3 (Table S1). Publication trends were divided into three phases. During the Initial Exploration Phase (1996–2004), research activity was minimal, with an average of only 1.7 publications per year. The Growth Phase (2005–2008) saw a modest increase, averaging five publications per year. During the Expansion Phase (2009–2017), MGV research increased significantly, with an average of 13.0 publications per year. The Acceleration Phase (2018–2024) exhibited a dramatic increase, with over 21 publications published annually.

In total, 13,533 citations were recorded, with an average of approximately 466.7 citations per year (Table S1). Notably, citations surged in 2008, peaking in 2009 at 1701. From 2009 to 2017, the annual average was sustained at 831 citations. After 2018, more than 356 citations were consistently observed per year. However, after 2018, although the number of publications increased substantially, average citations per article decreased (Figure 1). This reflects a time-lag effect, as newer publications have had less time to accumulate citations compared with earlier landmark works. After 2018, more than 356 citations were consistently observed per year. Among the 300 publications analyzed, 33 (11.0%) were highly cited (cited more than 100 times). The most cited publications were published in 2009 and received 441 citations. In contrast, nine publications (3.0%) had never been cited, and 80 publications (26.7%) were cited fewer than 10 times.

3.2. Citation Analysis of National Contributions to Research

To assess international contributions and collaborative patterns in MGV research, an analysis was conducted based on the affiliations of the corresponding coauthors in each publication. Researchers in 46 countries authored 300 MGV-related articles. The corresponding authors represented 33 countries, while the coauthors spanned 46 countries. The United States emerged as the most active contributor, with 65 publications (21.7% = 65/300) led by corresponding authors and 112 publications (20.7% = 112/541), including U.S.-based co-authors, accounting for approximately one-quarter of all publications. France made a significant contribution—42 publications (14.0% = 42/300) by corresponding authors and 77 publications (14.2% = 77/541) by co-authors—demonstrating both leadership and strong collaborative engagement. Germany (64 publications: 22 corresponding, 42 co-authored) and the United Kingdom (61 publications: 21 corresponding, 40 co-authored) also presented high research productivity across both author roles. In recent years, China (55 publications: 25 corresponding and 30 co-authored) and Japan (51 publications: 19 corresponding and 32 co-authored) have shown increasing investments and interest in MGV research. Other countries with notable contributions included Canada (44 publications), Norway (42), Israel (24), and South Korea (22), all of which actively participated in international research networks (Figure 2, Tables S2 and S3).

An annual trend analysis of MGV publications by country (Figure 3) reveals that the United States has shown a steady increase in publications since its first MGV publications in 2001, with rapid growth particularly evident in the 2010s. Notable years for U.S. output include 2011 (eight publications), 2018 (six publications), and 2020 (six publications). France began increasing its publication output in 2005, with a concentrated period of research activity between 2008 and 2018, producing two to five publications annually. China entered this field in 2009 and has seen substantial expansion since 2021. Based on the number of publications over the last five years (2020–2024), the United States led with 25 publications, followed by China (15), Japan (12), Germany (8), Norway (6), and South Korea and France, with five publications each (Table S4).

Both the total publications and average citations per publication were considered to further evaluate the impact of national research (Figure 4). The United States not only published 65 MGV publications but also recorded the highest total citation count, with an average of 58.8 citations per publication, indicating a strong research influence. France has published 42 publications with an average of 69.3 citations per publication, reflecting high research quality. Although the United Kingdom had fewer publications, it achieved a high average citation rate of 68.5, suggesting a substantial academic impact. In contrast, countries such as China, Japan, South Korea, and Brazil had a moderate number of publications but relatively low average citation counts, indicating the need for further growth in citation impact (Table S5).

3.3. Institutional Contributions to MGV Research

A total of 433 institutions were identified as having published research on MGVs, of which 30 published 10 or more. The top 20 institutions accounted for 30.3% (n = 91) of the total publications, indicating that only a few core institutions were leading the field (Figure 5). In terms of research productivity, the Centre National de la Recherche Scientifique (CNRS) was the most prolific, publishing 63 publications. This was followed by Aix-Marseille Université (n = 37), Sorbonne Université (n = 28), the University of Bergen (n = 22), and Kyoto University (n = 21). Notably, France’s major academic institutions, such as the CNRS, Aix-Marseille Université, and Sorbonne Université, ranked among the top contributors, indicating a strong national research network supported by interinstitutional collaboration and concentrated investment.

In terms of research impact measured by total citations, CNRS again led with 4022 citations, followed by Aix-Marseille Université (n = 2896), Sorbonne Université (n = 1431), Institut de Recherche pour le Développement (IRD, n = 1033), and Commissariat à l’énergie atomique et aux énergies alternatives (CEA, n = 1027). To assess the qualitative influence, the average number of citations per publication was analyzed. Aix-Marseille Université 237 recorded the highest average at 78.27 citations per publication, followed by CEA (n = 68.47), CNRS-INSB (Institut des Sciences Biologiques of the French National Centre for Scientific Research, n = 66.88), Plymouth Marine Laboratory (n = 64.33), CNRS (n = 63.84), and University of British Columbia (n = 60.83). In contrast, institutions such as Kyoto University (n = 19.48) and the University of Tennessee (n = 19.92), despite having relatively high publication counts, showed lower average citation rates, indicating a limited academic impact.

From a national perspective, France demonstrated leadership in both research output and influence, with contributions from diverse institutions, including the CNRS, Aix-Marseille Université, Sorbonne Université, IRD, CEA, and Assistance Publique-Hôpitaux de Marseille (Table S6). The United States is represented by several institutions, such as the Bigelow Laboratory for Ocean Sciences, the University of Tennessee, and the University of Hawaii, although their influence varies. The United Kingdom, with institutions such as the Plymouth Marine Laboratory and the Marine Biological Association, has produced high-quality research, despite fewer contributors. On the other hand, Japan and China were represented in the top institutions by only one major organization, Kyoto University and the Chinese Academy of Sciences, respectively, indicating a relatively limited overall impact.

An analysis of the annual publication trends for the top 10 MGV-publishing institutions (Figure 6) revealed that the CNRS entered the MGVs field in 2005 and has since published an average of approximately 3.5 publications per year. Aix-Marseille University began publishing in the same year, with an average of 2.5 publications annually, followed by Kyoto University (n = 2.33), Sorbonne University (n = 2.15), and CEA (n = 2.14), all of which showed strong productivity. However, the analysis of cumulative publications over the past five years (2020–2024) showed a slightly different pattern from the overall top 10 list (Table S7). The CNRS remained the most productive, with 14 publications, followed by Kyoto University (n = 13), CEA (n = 10), Max Planck Society (n = 7), and the University of Bergen (n = 6).

3.4. Analysis of Key Researchers

The productivity and impact of leading researchers in the field of MGV studies were analyzed (Figure 7, Table S8). Hiroyuki Ogata emerged as the most prolific author, publishing 30 publications. His work was cited 1177 times with an average of 39.23 citations per publication (c/p). Despite publishing only 15 publications, Claverie recorded the highest total citation count with 1771 citations, yielding an impressive average of 118.07 citations per publication, making him the most influential researcher in terms of qualitative impact. Similarly, Didier Raoult, with only seven publications, amassed 655 citations, averaging 93.57 citations per publication, demonstrating a strong track record for high-impact publications. Other highly influential researchers based on average citations per publication included William H. Wilson (n = 12, c/p = 68.92), Michael J. Allen (n = 8, c/p = 66.13), Curtis A. Suttle (n = 8, c/p = 60.13), Yves Desdevises (n = 9, c/p = 58.00), Assaf Vardi (n = 8, c/p = 57.58), Bernard La Scola (n = 13, c/p = 57.00), Evelyne Derelle (n = 7, c/p = 50.57), and Hervé Moreau (n = 12, c/p = 50.33). These researchers belong to a group characterized by a high qualitative influence within the MGV research community.

3.5. Number of MGV Publications by Web of Science Categories

Analysis of the disciplinary distribution of the 300 MGV-related publications based on the Web of Science categories revealed that the research spans a variety of scientific domains, although it is heavily concentrated in specific fields related to biology and environmental science (Table S9). The categories with the highest number of publications were microbiology (n = 111) and virology (n = 84), comprising more than 65% of the total, indicating a strong focus on microbial and viral research. The other major categories included multidisciplinary sciences (n = 42), ecology (n = 28), and marine and freshwater biology (n = 24). Additionally, active research was observed in the applied and molecular life sciences categories, such as biotechnology and applied microbiology (n = 21), genetics and hereditary science (n = 16), and biochemistry and molecular biology (n = 12).

3.6. Analysis of Author Keywords

Prior to conducting the author keyword analysis, synonymous terms such as giant virus, NCLDV, and nucleocytoplasmic large DNA virus were standardized under the recently accepted taxonomic term Nucleocytoviricota. This was done to improve consistency and interpretability by reflecting on the latest developments in viral classification. An analysis of author keywords from 300 MGV-related publications revealed over 100 unique terms. Among these, the 20 most frequently occurring keywords were selected for detailed analysis (Table S10). The most frequently used keywords were Nucleocytoviricota (n = 74), followed by marine viruses (n = 41), Phycodnaviridae (n = 35), metagenome (n = 28), and Mimivirus (n = 24). These top five keywords each appeared in over 20 publications and together accounted for approximately 19.8% of all keyword occurrences. Other frequently used terms (appearing in 10 or more publications) included algal virus (n = 20), Megavirales (n = 14), viral ecology (n = 14), algal bloom (n = 12), diversity (n = 11), viral diversity (n = 11), and Virome (n = 10). These terms represent a wide array of research directions, particularly in the context of viral taxonomy and ecology. Less frequently occurring yet thematically significant keywords (n = 7–9) included Prasinovirus, virophage, horizontal gene transfer, viral communities, algae, Coccolithovirus, DNA polymerase, and haptophyta. They are associated with specific viral types, host taxa, or molecular features.

To identify the main research themes within the field of MGVs, a keyword co-occurrence network analysis was conducted using author keywords extracted from the 300 analyzed publications. The analysis was performed using the VOSviewer software, which visualizes the co-occurrence frequency of keywords mentioned together within the same articles (Figure 8). In the visualized network, each node represents an individual keyword, and the edges (connecting lines) represent co-occurrence relationships. The size of a node corresponds to the frequency of the keyword, whereas the color indicates the thematic cluster identified by the clustering algorithm of the software. In addition to the co-occurrence network analysis, a keyword density visualization was performed using VOSviewer to assess the frequency and relative importance of terms in MGV research (Figure S2). In this heatmap, warmer colors (red/orange) indicate highly frequent keywords such as Nucleocytoviricota, Marine virus, and Phycodnaviridae, whereas cooler colors (green/blue) represent less frequent terms. This visualization highlights the central role of taxonomy and ecology in MGV research, while also indicating emerging themes related to host–virus interactions, genomic functions, and methodological advances.

Nucleocytoviricota was identified as the central node, frequently co-occurring with marine viruses, Phycodnaviridae, and the metagenome. The keywords were categorized into four major thematic clusters. The blue cluster is centered on Nucleocytoviricota and includes terms such as Mimivirus, Megavirales, virophage, and protist, reflecting research focused on MGVs and their interactions with virophages and protists.

The orange cluster, anchored by marine viruses, encompasses keywords such as diversity, horizontal gene transfer, transcriptome, and viral–host interactions, highlighting studies on genetic diversity, functional roles, and complex interactions between viruses and their hosts. The pink cluster included Phycodnaviridae, an algal virus, Prasinovirus, and viral ecology, indicating an intensive research focus on algal viruses and their ecological functions in marine ecosystems. Finally, the green cluster featured keywords, such as metagenome, virome, viral communities, and microbiome, underscoring the growing importance of metagenomic and viromic approaches for investigating the composition and diversity of marine viral assemblages. Overall, the network reveals a multifaceted field with interrelated but distinct research directions, each contributing to a broader understanding of MGVs.

An analysis of author keywords from studies on MGVs published between 1996 and 2024 was conducted to examine the evolution of the research themes over time (Figure 9). Across the entire period, the most frequently used keywords were Nucleocytoviricota (n = 74), marine viruses (n = 41), Phycodnaviridae (n = 35), metagenome (n = 28), and Mimivirus (n = 24). The research period was divided into four distinct phases, each reflecting a shift in thematic focus. Phase 1 (1996–2004) marked the initial stage of marine giant virus research, primarily featuring keywords associated with known algal viruses and their host organisms, such as Phycodnaviridae (n = 6), algal viruses (n = 5), algae (n = 2), and marine viruses (n = 1). In Phase 2 (2005–2008), studies began to explore the genomics and taxonomy of giant viruses, as evidenced by the emergence of new keywords, including Nucleocytoviricota (n = 2), diversity (n = 1), Coccolithovirus (n = 1), and DNA polymerase (n = 1). Phase 3 (2009–2017) witnessed a significant expansion in research activity driven by technological advancements, with the frequent appearance of keywords such as metagenome (n = 11), Mimivirus (n = 9), Megavirales (n = 7), horizontal gene transfer (n = 7), viral diversity, virome, Prasinovirus, and virophage. Finally, Phase 4 (2018–2024) showed a substantial increase in the frequency of core research terms, although this was not marked by the introduction of new keywords. In particular, Nucleocytoviricota (n = 45), metagenome (n = 17), viral ecology (n = 9), algal blooms (n = 8), virophages (n = 7), and viral communities (n = 7) became prominent, highlighting the growing and sustained interest of researchers in these areas.

A comparison of the top 10 most frequently used author keywords in the overall period (1996–2024) versus the most recent five years (2020–2024) is presented in Table S11. Throughout the full time span, the top keywords were Nucleocytoviricota (n = 74), marine virus (n = 41), Phycodnaviridae (n = 35), metagenome (n = 28), and Mimivirus (n = 24). In contrast, during the most recent five years, Nucleocytoviricota (n = 37) remained the most frequently used keyword, followed by marine viruses (n = 10), metagenome (n = 10), viral ecology (n = 7), and Mimivirus (n = 6). Notably, keywords such as algal bloom, viral diversity, virophages, and viromes also emerged among the top terms in the recent period.

4. Discussion

4.1. Research Development Stages and Technological Advances by Year

MGV research has undergone four broad developmental stages. The first stage (1996–2003) was a period of low awareness of giant viruses, with most studies limited to sporadic observations of marine viruses or reports of diseases in marine algae [40]. During this time, there was a lack of systematic understanding of the ecological importance and taxonomic position of MGVs. The second stage (2004–2008) was catalyzed by the genomic analysis of Mimivirus [41], which sparked increased interest in giant viruses. The discovery of new viruses, such as Sputnik virophages [25] and Cafeteria roenbergensis virus [17], initiated a more active exploration of the role of giant viruses within marine microbial communities. The third stage (2009–2017) saw explosive growth in research due to advancements in metagenomics, single-virus genomics, and the emergence of large-scale expedition projects, such as the Tara Oceans [26,42] and the Global Ocean Virome project [11,27]. During this period, integrated analyses of viral community structure, evolution, and ecological functions became possible. In 2018, the field entered the fourth stage, with more than 25 publications published annually, reaching quantitative and qualitative peaks. In particular, research has been conducted to establish a taxonomy of Nucleocytoviricota [21,43,44], virus-host interactions, and virus-mediated carbon cycling regulation [22,45].

4.2. Citation Analysis and Key Publications

Citation analysis in the field of MGVs is an important tool for surveying major research trends, core topics, and scholarly achievements. The importance of these landmark contributions is further underscored in Supplementary Table S12, which lists the ten most cited publications between 1996 and 2024. These studies—ranging from the discovery of Mimivirus and virophages to large-scale metagenomic surveys such as Tara Oceans—represent pivotal turning points in redefining viral taxonomy, ecology, and evolutionary significance. Highly cited publications generally correspond to turning points in research paradigms or technical innovations, deepening our understanding of marine viral ecosystems. For example, Rohwer and Thurber [46] suggested that viruses function not merely as pathogens but as regulators of biogeochemical cycling, gene flow, and host diversity in marine microbial ecosystems, promoting an ecological paradigm shift in MGV research. This publication was cited 441 times as of 2024, becoming a classically influential work in this field. Additionally, Hingamp et al. [26], part of the Tara Oceans project, analyzed the functional contribution of giant viruses based on viral gene expression data within marine plankton communities. This study is regarded as one of the first to quantitatively present MGV activity at the transcriptome level, contributing to the scientific visualization of the “invisible functionality” of viruses. Endo et al. [10] utilized data from Global Ocean Virome 2.0 (GOV2.0) to perform a large-scale analysis of the ecological niches and virus–host interactions of the Nucleocytoviricota lineage distributed globally in the ocean. This study opens new avenues in marine viral biogeography by linking phylogenetic diversity, geographic distribution, and functional gene composition. More recently, Zayed, et al. [12] reconstructed thousands of marine virus metagenome-assembled genomes to explore unknown viral genomes and predictive modeling of gene functions, significantly contributing to the understanding of viral phylogeny and environmental adaptation. These key publications support the paradigm shift in recognizing marine viruses as not only infectious agents, but also ecosystem regulators and genetic resource providers, clearly indicating multidisciplinary expansion and technological convergence in MGV research.

4.3. Research Trends by Country and Institution

The analysis of research productivity and collaboration networks at the country and institutional levels is crucial for understanding the geographic centrality, research focus, and collaboration structure in MGV research. This study found that the United States and France occupy leading positions in MGV research, with notable activities emerging in major European countries, Japan, and, more recently, China and South Korea.

France has formed a research cluster centered on institutions such as (Centre National de la Recherche Scientifique), Aix-Marseille Université, and Sorbonne Université. The CNRS ranks at the top in terms of both the number of publications (63 publications) and citations (over 4000). Aix-Marseille Université stands out as a representative institution for high-quality research with an average citation count per publication of 78.27. These institutions, led by researchers such as Claverie, Raoult, Abergel, and Legendre, have made significant contributions to Mimivirus and Pandoravirus genome research, the discovery of virophages, and the establishment of viral taxonomy [47,48].

The United States has established itself as a global leader in marine metagenomics and viral ecology research, with active studies conducted in prominent institutions, including Ohio State University, the University of Arizona, Massachusetts Institute of Technology (MIT), and the Bigelow Laboratory for Ocean Sciences. Researchers, such as Matthew B. Sullivan, Forest Rohwer, Holly M. Simon Steward, and Héctor A. Ignacio-Espinoza, have played key roles in the Tara Oceans and Global Ocean Virome projects, significantly contributing to the collection, refinement, and analytical infrastructure of extensive marine viral ecology datasets [11,49]. Through high-resolution metagenomic and metatranscriptomic analyses, these researchers have laid an important academic foundation for elucidating the diversity and functions of marine viruses, as well as the complex interaction mechanisms with their hosts. Furthermore, their work has been central to a comprehensive understanding of the biogeochemical roles of marine viruses and the geographic and environmental distribution patterns of viral communities.

Japan’s Kyoto University and Japan Agency for Marine-Earth Science and Technology have played important roles in mimivirus-related taxonomic research and ecological characterization [50]. In particular, these institutions have investigated the infection and interaction mechanisms between giant viruses and marine microalgal hosts, such as protists and algae, thereby enhancing the understanding of virus–host dynamics and their ecological impacts. This study provides essential data for assessing the influence of marine viruses on microalgal community regulation and marine carbon cycling.

4.4. Evolution of Key Themes: Function, Interaction, and Environmental Integration

Our keyword analysis demonstrated that MGV research has evolved from a focus on specific viral classifications to broader investigations encompassing ecological functions, virus–host interactions, and environmental linkages. In early studies, keywords such as Phycodnaviridae, Mimivirus, and Megavirales, which were taxonomically defined, were predominant. Since the mid-2000s, the introduction of ICTV reclassification under Nucleocytoviricota has prompted a more systematic taxonomic restructuring [44]. Subsequent research has shifted attention toward the functional and ecological roles of viruses, with keywords such as algal virus, Coccolithovirus, and Prasinovirus indicating increased interest in virus-induced lysis of microalgal hosts and their implications for the marine carbon cycle [22,51]. Notably, host cell lysis triggered by viral infection contributes to dissolved organic matter release, which supports microbial loop energy redistribution—a concept captured in the “viral shunt” hypothesis [52].

More recently, the emergence of keywords such as virophages, viral–host interactions, and co-infections reflects the growing interest in the interactions between giant viruses and virophages, multiple infection dynamics, and intra-host viral regulatory mechanisms [30,53]. These interactions extend beyond simple pathogenicity to encompass the ecological stability and survival dynamics of the protist hosts. Additionally, keywords such as metagenome, virome, Tara Oceans, and Global Ocean Virome indicate the broadening of MGV research to integrative analyses based on large-scale environmental meta-omics datasets that explore viral diversity, spatial distribution, and functional gene expression [12,42]. This expansion, enabled by high-throughput sequencing and metagenome-assembled genome reconstruction, has contributed significantly to resolving spatiotemporal patterns and environmental associations of global oceanic viral communities. In summary, keywords related to MGVs have evolved from those focused on viral discovery to those that emphasize functional elucidation and environmental network analysis, indicating a strong link to future research trajectories.

4.5. Future Perspectives

Although research on MGVs remains relatively nascent, it is expected to expand rapidly through technological advancements and interdisciplinary approaches. First, artificial intelligence (AI)-based methods for gene function prediction and virus-host interaction modeling are expected to flourish. Recent developments—such as AlphaFold, DeepFRI, and GPT4-mol—are overcoming the limitations of traditional homology-based annotation by enabling functional interpretation of previously unknown “dark matter” genes [54,55]. These technologies are expected to provide breakthroughs in deciphering the functions of non-coding or uncharacterized genes in MGV genomes and in predicting network-based interactions.

Second, the geographical scope of the research is likely to extend beyond surface oceans to include deep-sea, polar, and hypersaline environments. Extreme habitats such as hydrothermal vents and subglacial polar waters are recognized as reservoirs of novel viral ecosystems, potentially offering insights into traditional marine microbiology [56].

Third, a paradigm shift is being discussed in viral taxonomy from a strictly phylogenetic approach to one based on functional ecotypes. This involves classifying viruses based on their ecological roles, host ranges, and environmental niches, thus facilitating a more integrated understanding of viral ecology and evolution [21].

Fourth, the industrial application potential of genes and proteins derived from giant viruses is gaining increasing attention. Functional genes such as DNA polymerases, RNA polymerases, and nucleases can be applied in next-generation gene editing, diagnostic kits, and synthetic biology platforms, thus enhancing the prospects of marine viral resources in biotechnology [57].

Fifth, the establishment of a global ocean viral surveillance and monitoring system is urgently required. Follow-up studies on international expeditions, such as the Tara Oceans and Global Ocean Virome, as well as region-specific long-term programs, such as the Polar Virome Initiative and Deep Ocean Virome Consortium, could serve as early warning systems for climate change, biodiversity loss, and the emergence of pathogenic marine viruses.

In conclusion, research on marine giant viruses is rapidly expanding beyond taxonomy toward functional interpretation, ecological integration, and industrial applications. This trajectory is poised to make significant contributions not only to our understanding of marine ecosystems but also to the broader fields of life sciences.

4.6. Limitations

This study has several limitations. First, the analysis was restricted to the Web of Science Core Collection; thus, relevant publications in Scopus, PubMed, or Google Scholar may not have been included. Second, citation-based indicators inherently suffer from the time-lag effect, leading to underestimation of the influence of more recent works. Third, bibliometric results depend on the accuracy of author-supplied metadata and keywords, which may introduce classification biases. Despite these limitations, the present study provides a robust and systematic overview of the structural evolution and collaborative landscape of marine giant virus research.

5. Conclusions

This study conducted a scientometric analysis of MGV research based on publications indexed in the Web of Science Core Collection between 1996 and 2024. The results show that MGV-related publications accounted for approximately 19.4% of all giant virus studies, indicating the growing academic significance of MGVs in marine microbial ecosystems.

Chronologically, MGV research gained momentum following the discovery of the mimivirus in 2004. Major international initiatives, such as the Tara Oceans and Global Ocean Virome, alongside advances in high-throughput metagenomic technologies, have served as key drivers for the rapid expansion of this field. Citation analyses have highlighted seminal works, such as Rohwer and Thurber [46], Hingamp et al. [26], and Endo et al. [10], which have provided critical turning points in elucidating the ecological functions of marine viruses, gene network analyses, and biogeographical diversity. At national and institutional levels, France’s CNRS, U.S. institutions such as Bigelow Laboratory for Ocean Sciences and the University of Hawaii, and Japan’s Kyoto University have emerged as leading research hubs. Although participation in China and South Korea is increasing, limitations on international collaboration remain. Keyword analyses revealed a shift in focus from simple viral taxonomy to function- and interaction-oriented research, as evidenced by the prominence of terms such as “viral-host interaction,” “virophage,” “metagenome,” and “carbon cycle.”

Looking ahead, MGV research is expected to evolve rapidly along several fronts, including AI-based functional gene prediction, exploration of viral ecosystems in extreme environments, establishment of ecotype-based classification systems, industrial utilization of viral genes, and the development of global long-term viral observation networks. This expanding research landscape has the potential to deepen our understanding of marine ecosystems and open new frontiers in life sciences and biotechnology industries.

6. Patents

This section is not mandatory but may be added if there are patents resulting from the work reported in this manuscript.