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Cophylogeny and convergence shape holobiont evolution in sponge–microbe symbioses

Abstract

Symbiotic microbial communities of sponges serve critical functions that have shaped the evolution of reef ecosystems since their origins. Symbiont abundance varies tremendously among sponges, with many species classified as either low microbial abundance (LMA) or high microbial abundance (HMA), but the evolutionary dynamics of these symbiotic states remain unknown. This study examines the LMA/HMA dichotomy across an exhaustive sampling of Caribbean sponge biodiversity and predicts that the LMA symbiotic state is the ancestral state among sponges. Conversely, HMA symbioses, consisting of more specialized microorganisms, have evolved multiple times by recruiting similar assemblages, mostly since the rise of scleractinian-dominated reefs. Additionally, HMA symbioses show stronger signals of phylosymbiosis and cophylogeny, consistent with stronger co-evolutionary interaction in these complex holobionts. These results indicate that HMA holobionts are characterized by increased endemism, metabolic dependence and chemical defences. The selective forces driving these patterns may include the concurrent increase in dissolved organic matter in reef ecosystems or the diversification of spongivorous fishes.

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Fig. 1: Caribbean sponge holobiont dataset is consistent across sites and sufficient to detect phylum-wide trends in the evolutionary dynamics of microbial symbioses.
Fig. 2: HMA and LMA microbial communities exist as discrete states.
Fig. 3: HMA sponge microbial communities are highly specialized.
Fig. 4: The dynamic evolutionary history of HMA and LMA sponges.
Fig. 5: Correlated evolution of chemical defences and HMA symbioses.
Fig. 6: Patterns of phylosymbiosis in sponges are driven by HMA holobionts.

Data availability

The sponge barcoding data for 18S and COI markers are accessioned at GenBank under MZ416255MZ416736 and MZ486496MZ487633, respectively. The microbial 16S MiniSeq reads and metagenomic libraries are available through the NCBI Short Read Archive under BioProject PRJNA555077.

Code availability

The complete bioinformatic pipeline including scripts for figure reproduction is available through the GitHub repository at https://github.com/scriptomika/SpongeDOB.

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Acknowledgements

We thank E. Kintzing, K. Morrow, A. C. Abraham, A. Chaves-Fonnegra and B. Mueller for help with sample collection. The samples were collected under the following permits: Belize Marine Scientific Research Permit Number 000034-17, Virgin Islands Division of Fish and Wildlife Research/Export Permit DFW18078X, Curaçao Scientific Collection Permit 2012/48584 and a Cayman Islands Government Department of Environment Research Permit. Logistical support was provided by the CARMABI Foundation in Curaçao, the Smithsonian Caribbean Coral Reef Ecosystems Program’s Carrie Bow Cay Marine Field Station in Belize, the University of the Virgin Islands in St. Croix and the staff of InDepth Water Sports in Grand Cayman. We thank the Hubbard Center for Genome Studies and the Research Computing Center (University of New Hampshire) for access to the Premise high-performance cluster. This project was funded by National Science Foundation Dimensions of Biodiversity grants OCE-1638296/1638289 and Biological Oceanography Program grants OCE-1632348/1632333 to the University of New Hampshire and the University of Mississippi, respectively.

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M.S.P., K.J.M., D.J.G., M.S. and M.P.L. collected the specimens. M.S.P., K.J.M. and M.G. performed the molecular work. M.S.P. analysed the data. M.S.P., D.C.P. and M.P.L. wrote the manuscript. All authors reviewed the manuscript.

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Correspondence to M. Sabrina Pankey.

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Nature Ecology & Evolution thanks Ute Hentschel, Ryan McMinds and the other, anonymous, reviewer(s) for their contribution to the peer review of this work. Peer reviewer reports are available.

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Extended data

Extended Data Fig. 1 Specimen sampling summary.

Barplots summarizing numbers of specimens collected at each locale representing unique species, corroborated by sponge barcode data.

Extended Data Fig. 2 Phylogenetic identification of newly collected sponge samples.

Supermatrix phylogeny inferred from nucleotide housekeeping genes and GenBank reference taxa. Clades are labeled according to taxonomy (World Porifera Database), with non-monophyletic groups indicated.

Extended Data Fig. 3 Data occupancy for supermatrix phylogeny.

Circular tree (identical to Extended Data Fig. 2) with rings indicating which housekeeping markers were used. From interior to outer rings: 1) ATP synthase F1 beta (ATPB); 2) nuclear fructose-bisphosphate aldose (Ald1); 3) catalase (Cat); 4) mitochondrial cytochrome oxidase I (COI); 5) methionine adenosyltransferase (Mat1); 6) 6-phosphofructokinase (Pfk); 7) ribosomal subunit 18 S; and 8) triosephosphate isomerase (Tpi).

Extended Data Fig. 4 Fossil-calibrated species-level sponge phylogeny.

Geological time represented by colored boxes detailed in legend. Support values shown for bipartitions on species phylogeny, using IQ-TREE ultrafast bootstrapping method. Topological constraints are shown in red and represent bipartitions present in phylogeny inferred from the species tree based on transcriptomic data and received 100% bootstrap support (inset). Species for which bacterial densities have been previously empirically or computationally derived are annotated with blue (LMA) or orange (HMA) dots. Species for which palatability assays are available are indicated with an asterisk. Numbers represent the number of specimens recovered in this study for each species.

Extended Data Fig. 5 Chronogram of sponge species phylogeny based on fossil calibrations.

Distant outgroups have been omitted to improve visual resolution of timescales. Clades are labeled according to taxonomy (World Porifera Database), with non-monophyletic groups indicated.

Extended Data Fig. 6 HMA holobionts demonstrate greater metabolic syntrophism than LMA holobionts.

Proportional library read contributions of host (left) and microbial community (right) biochemical pathways, estimated from metagenomic datasets for replicates of three HMA and two LMA species (45 metagenomic datasets in total). HMA sponge host genomes have comparatively less functional capacity than LMA host genomes. Conversely, in most cases, HMA symbiont genomes have more functional capacity than LMA symbiont genomes (left). Rare pathways that are overrepresented by LMA symbiont genomes are shown in bold.

Extended Data Fig. 7 Strength of random effect terms in pGLMM models of microbial phyletic abundances.

Intra-class correlation coefficients for all model terms in pGLMM run for each microbial group. ICC values (y-axis) are plotted against a metric representing the degree to which a given microbial group is enriched in HMA or LMA sponges (ln (proportional abundance)). Model terms included in each pGLMM include A) Geography, B) interaction between host and symbiont phylogenies (co-diversification), as well as interactive effects of microbial phylogeny with host identity (C) and host phylogeny with microbial identity (D).

Extended Data Fig. 8 Cophylogeny characterizes the evolution of HMA sponges.

Diagnostic HMA and LMA microbial taxa are plotted by interclass correlation scores (ICC) for co-evolutionary interaction (y-axis) and enrichment in either HMA or LMA sponges (x-axis). Microbial taxa diagnostic of HMA sponges show significantly greater phylogenetic interaction with sponge phylogeny. (B) Multiple instances of cophylogeny between clades of Dehalococcoidia (an HMA-diagnostic class of Chloroflexi) and sponges of Order Agelasida. Heatmap shows abundance (relative to overall microbiome) of each Chloroflexi variant (columns) across sampled agelasid sponge species (rows). Corresponding sponge and microbial phylogenies shown at left and bottom, respectively. Microbial tree tips colored by Order of sponge host inhabited.

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Sabrina Pankey, M., Plachetzki, D.C., Macartney, K.J. et al. Cophylogeny and convergence shape holobiont evolution in sponge–microbe symbioses. Nat Ecol Evol 6, 750–762 (2022). https://doi.org/10.1038/s41559-022-01712-3

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