Seq’ and ARMS shall find: DNA (meta)barcoding of Autonomous Reef Monitoring Structures across the tree of life uncovers hidden cryptobiome of tropical urban coral reefs

Abstract

Coral reefs are among the richest marine ecosystems on Earth, but there remains much diversity hidden within cavities of complex reef structures awaiting discovery. While the abundance of corals and other macroinvertebrates are known to influence the diversity of other reef‐associated organisms, much remains unknown on the drivers of cryptobenthic diversity. A combination of standardized sampling with 12 units of the Autonomous Reef Monitoring Structure (ARMS) and high‐throughput sequencing was utilized to uncover reef cryptobiome diversity across the equatorial reefs in Singapore. DNA barcoding and metabarcoding of mitochondrial cytochrome c oxidase subunit I, nuclear 18S and bacterial 16S rRNA genes revealed the taxonomic composition of the reef cryptobiome, comprising 15,356 microbial ASVs from over 50 bacterial phyla, and 971 MOTUs across 15 metazoan and 19 non‐metazoan eukaryote phyla. Environmental factors across different sites were tested for relationships with ARMS diversity. Differences among reefs in diversity patterns of metazoans and other eukaryotes, but not microbial communities, were associated with biotic (coral cover) and abiotic (distance, temperature and sediment) environmental variables. In particular, ARMS deployed at reefs with higher coral cover had greater metazoan diversity and encrusting plate cover, with larger‐sized non‐coral invertebrates influencing spatial patterns among sites. Our study showed that DNA barcoding and metabarcoding of ARMS constitute a valuable tool for quantifying cryptobenthic diversity patterns and can provide critical information for the effective management of coral reef ecosystems.

Hierarchical drivers of cryptic biodiversity on coral reefs

“…How predators respond to enhanced resource availability along this trajectory could be addressed using extended size spectra analyses (Heather et al, 2021) from cryptobenthic predators (Mihalitsis et al, 2022) to large higher order predators beyond the benthos. The knowledge gained here would benefit from the increased taxonomic resolution of sessile taxa and motile cryptofauna. There are extreme taxonomic constraints in the cryptofauna, yet molecular and environmental DNA metabarcoding techniques are growing in popularity to partition cryptic community structures (Carvalho et al, 2019; Ip et al, 2022; Leray & Knowlton, 2015; Pearman et al, 2018; Plaisance et al, 2009). These approaches seem important to employ in the context of the ecological outcomes presented from microhabitat to seascape here. The intermediate disturbance hypothesis (Connell, 1978; Dial & Roughgarden, 1998) may help to explain the nonstructured seascape patterns in the cover of sessile taxa and motile cryptofauna density observed here, which were greatest in the mid‐exposure site.…”

“…The knowledge gained here would benefit from the increased taxonomic resolution of sessile taxa and motile cryptofauna. There are extreme taxonomic constraints in the cryptofauna, yet molecular and environmental DNA metabarcoding techniques are growing in popularity to partition cryptic community structures (Carvalho et al, 2019;Ip et al, 2022;Leray & Knowlton, 2015;Pearman et al, 2018;Plaisance et al, 2009). These approaches seem important to employ in the context of the ecological outcomes presented from microhabitat to seascape here.…”

Insights into Ecological & Evolutionary Processes via community metabarcoding

“…In this case, diversity measures could thus not be used as a proxy for ecological importance. Finally, Ip, Chang, Oh, et al (2022) combine standardised sampling using Autonomous Reef Monitoring Structures (ARMS) and high-throughput sequencing to test whether coral cover shapes diversity patterns among organisms inhabiting hidden spaces within the reef matrix (the "cryptobiome"). They showed that, while marine fungi, bacteria, phytoplankton and other planktonic organisms were impacted primarily by abiotic factors (depth, temperature, level of particles in the water column and distance from the mainland), diversity patterns in larger-sized metazoans were associated with coral cover.…”

Editorial 2024

“…Finally, our third Special Issue, Insights into Ecological & Evolutionary Processes via Community Metabarcoding includes ‘papers that highlight the power of high‐throughput sequencing (HTS) data to address classic questions in ecology and evolution, particularly focused on metabarcoding (amplicon) datasets in conjunction with complementary ‐omics data types and/or models/theory to infer overall ecosystem processes’ (Gillespie et al., 2023). The impressive collection of 44 manuscripts covers a wide range of topics: community assembly processes (Andujar et al., 2022; Arjona et al., 2022; Emerson et al., 2022; Govender et al., 2022; Guerrieri et al., 2022; Ip, Chang, Oh, et al., 2022; Kiemel et al., 2022; Li et al., 2022; Macheriotou et al., 2023; Menéndez‐Serra et al., 2023; Nappi et al., 2022; Noguerales et al., 2023; Overcast et al., 2023; Pino et al., 2023; Van der Loos et al., 2022; Wang et al., 2022), interaction networks (Ando et al., 2022; Bell et al., 2022; Dürrbaum et al., 2022; Encinas‐Viso et al., 2022; Ficetola & Taberlet, 2023; Graham et al., 2022; Ip, Chang, Tun, et al., 2022; Lowe et al., 2022; Lu et al., 2022; Lue et al., 2022; Pitteloud et al., 2022; Srivathsan et al., 2022; Tommasi et al., 2022), cross‐scale interactions and microbiomes (Brinker et al., 2022; Câmara dos Reis et al., 2022; Hu et al., 2022; Kivistik et al., 2022; Manthey et al., 2022; Merges et al., 2022; Michel et al., 2022; Molina et al., 2022; Navine et al., 2022; Pereira et al., 2022; Perez‐Lamarque & Morlon, 2022; Rolshausen et al., 2022), and invasive species/homogenization (Andrés et al., 2023; Graham et al., 2022; Hampel et al., 2022; Kennedy et al., 2022; Overcast et al., …”

“…Collectively the articles in this Special Issue 'underline the huge impact of the anthropogenic environment in microbial evolution, including the emergence and spread of pathogens as well as the benefits provided by domesticated or mutualistic fungi and bacteria'(Giraud et al, 2023).Finally, our third Special Issue, Insights into Ecological & Evolutionary Processes via Community Metabarcoding includes 'papers that highlight the power of high-throughput sequencing (HTS) data to address classic questions in ecology and evolution, particularly focused on metabarcoding (amplicon) datasets in conjunction with complementary -omics data types and/or models/theory to infer overall ecosystem processes'(Gillespie et al, 2023). The impressive collection of 44 manuscripts covers a wide range of topics: community assembly processes(Andujar et al, 2022;Arjona et al, 2022;Emerson et al, 2022;Govender et al, 2022;Guerrieri et al, 2022;Ip, Chang, Oh, et al, 2022;Kiemel et al, 2022;Li et al, 2022;Macheriotou et al, 2023;Menéndez-Serra et al, 2023;Nappi et al, 2022;Noguerales et al, 2023;Overcast et al, 2023;Pino et al, 2023;Van der Loos et al, 2022;Wang et al, 2022), interaction networks(Ando et al, 2022;Bell et al, 2022;Dürrbaum et al, 2022;Encinas-Viso et al, 2022;Ficetola & Taberlet, 2023;Graham et al, 2022;Ip, Chang, Tun, et al, 2022;Lowe et al, 2022;Lu et al, 2022;Lue et al, 2022;Pitteloud et al, 2022;Srivathsan et al, 2022;Tommasi et al, 2022), cross-scale interactions and microbiomes(Brinker et al, 2022;Câmara dos Reis et al, 2022...…”