Contrasting drivers of abundant phage and prokaryotic communities in tropical, coastal ecosystems across the Isthmus of Panama

Phages, or viruses that infect bacteria and archaea, are ubiquitous and abundant members of Earth′s ecosystems that impact the flow of nutrients, evolution of microbes, and food web dynamics by selectively infecting and killing their prokaryotic hosts. Because phages can only replicate through their hosts, they are inherently linked to processes impacting their hosts′ distribution and susceptibility to infection. Despite these links, phages can also be affected by environmental parameters independent of their hosts, such as pH or salinity which impact cell adsorption or virion degradation. To understand these complex links, in this study, we leverage the unique ecological context of the Isthmus of Panama, which narrowly disconnects the productive Tropical Eastern Pacific (TEP) and Tropical Western Atlantic (TWA) provinces and compare factors that shape active marine phage and prokaryotic communities. Metagenomic sequencing of seawater from mangroves and reefs of both the TEP and TWA coasts of Panama suggest that pronounced environmental gradients, such as along the TEP mangrove rivers, result in common dispersal and physicochemical parameters shaping both prokaryotic and phage community composition and diversity. Conversely, we find that when environmental conditions are relatively similar across adjacent habitats, such as between the mangroves and reefs in the TWA, prokaryotic communities are more influenced by local abiotic conditions while phage communities are shaped more by dispersal. Collectively, this work provides a framework for addressing the co-variability between viruses and their hosts in marine systems and for identifying the different factors that drive consistent versus disparate trends in community shifts, which is essential to inform models of these interactions in biogeochemical cycling.

The gut microbiome variability of a butterflyfish increases on severely degraded Caribbean reefs

Environmental degradation has the potential to alter key mutualisms that underlie the structure and function of ecological communities. How microbial communities associated with fishes vary across populations and in relation to habitat characteristics remains largely unknown despite their fundamental roles in host nutrition and immunity. We find significant differences in the gut microbiome composition of a facultative coral-feeding butterflyfish (Chaetodon capistratus) across Caribbean reefs that differ markedly in live coral cover (∼0–30%). Fish gut microbiomes were significantly more variable at degraded reefs, a pattern driven by changes in the relative abundance of the most common taxa potentially associated with stress. We also demonstrate that fish gut microbiomes on severely degraded reefs have a lower abundance of Endozoicomonas and a higher diversity of anaerobic fermentative bacteria, which may suggest a less coral dominated diet. The observed shifts in fish gut bacterial communities across the habitat gradient extend to a small set of potentially beneficial host associated bacteria (i.e., the core microbiome) suggesting essential fish-microbiome interactions may be vulnerable to severe coral degradation.

MIDORI2: A collection of quality controlled, preformatted, and regularly updated reference databases for taxonomic assignment of eukaryotic mitochondrial sequences

Analysis of environmental DNA is increasingly used to characterize ecological communities, but the effectiveness of this approach depends on the accuracy of taxonomic reference databases. The MIDORI databases, first released in 2017, were built to improve accuracy for mitochondrial metazoan (animal) sequences. MIDORI has now been significantly improved and renamed MIDORI2 (available at Like MIDORI, MIDORI2 is built from GenBank and contains curated sequences of thirteen protein-coding and two ribosomal RNA mitochondrial genes. Coverage has been substantially expanded to cover all eukaryotes, including fungi, green algae and land plants, other multicellular algal groups, and diverse protist lineages. MIDORI2 also now includes not only species with full binomials, but also taxa referred to by genus with species left unspecified (“sp.”). Another new feature is the updating of the databases approximately every two months with version numbers corresponding to each new GenBank release. Additional potentially erroneously annotated sequences have also been removed. Finally, the ability to export data files to BLAST+ has been added to the original ability to export preformatted data to five taxonomic assignment programs, and databases of amino acid sequences are also made available for protein-coding genes. As a technical validation, we conducted a preliminary comparison of the performance of MIDORI2 with five taxonomic assignment programs. Results suggest that BLAST+ top hits performed better for assigning CO1 sequences than alignment-free methods based on compositional features. Comparing MIDORI2 with two other commonly used curated databases of mitochondrial sequences, CO-ARBitrator and BOLD, we show that MIDORI2 includes sequences from a broader range of metazoan and non-metazoan taxa. Overall, in many contexts, MIDORI2 offers clear advantages–a higher diversity of taxa than other databases, a variety of user-friendly features, and regular updates. MIDORI2 is particularly well-suited for environmental DNA studies that target mitochondrial genes with broad primers.

Natural experiments and long-term monitoring are critical to understand and predict marine host–microbe ecology and evolution

Marine multicellular organisms host a diverse collection of bacteria, archaea, microbial eukaryotes, and viruses that form their microbiome. Such host-associated microbes can significantly influence the host’s physiological capacities; however, the identity and functional role(s) of key members of the microbiome (“core microbiome”) in most marine hosts coexisting in natural settings remain obscure. Also unclear is how dynamic interactions between hosts and the immense standing pool of microbial genetic variation will affect marine ecosystems’ capacity to adjust to environmental changes. Here, we argue that significantly advancing our understanding of how host-associated microbes shape marine hosts’ plastic and adaptive responses to environmental change requires (i) recognizing that individual host–microbe systems do not exist in an ecological or evolutionary vacuum and (ii) expanding the field toward long-term, multidisciplinary research on entire communities of hosts and microbes. Natural experiments, such as time-calibrated geological events associated with well-characterized environmental gradients, provide unique ecological and evolutionary contexts to address this challenge. We focus here particularly on mutualistic interactions between hosts and microbes, but note that many of the same lessons and approaches would apply to other types of interactions.

Global biogeography of chemosynthetic symbionts reveals both localized and globally distributed symbiont groups

In the ocean, most hosts acquire their symbionts from the environment. Due to the immense spatial scales involved, our understanding of the biogeography of hosts and symbionts in marine systems is patchy, although this knowledge is essential for understanding fundamental aspects of symbiosis such as host–symbiont specificity and evolution. Lucinidae is the most species-rich and widely distributed family of marine bivalves hosting autotrophic bacterial endosymbionts. Previous molecular surveys identified location-specific symbiont types that “promiscuously” form associations with multiple divergent cooccurring host species. This flexibility of host–microbe pairings is thought to underpin their global success, as it allows hosts to form associations with locally adapted symbionts. We used metagenomics to investigate the biodiversity, functional variability, and genetic exchange among the endosymbionts of 12 lucinid host species from across the globe. We report a cosmopolitan symbiont species, Candidatus Thiodiazotropha taylori, associated with multiple lucinid host species. Ca. T. taylori has achieved more success at dispersal and establishing symbioses with lucinids than any other symbiont described thus far. This discovery challenges our understanding of symbiont dispersal and location-specific colonization and suggests both symbiont and host flexibility underpin the ecological and evolutionary success of the lucinid symbiosis.

Two new species of Typton Costa, 1844 from tropical American waters, with taxonomic notes on T. tortugae McClendon, 1911 and a new record of T. granulosus Ayón-Parente, Hendrickx & Galvan-Villa, 2015 (Decapoda: Caridea: Palaemonidae)

Two new species of the palaemonid shrimp genus Typton Costa, 1844 are described based on material from Panama and Mexico. Both species are closely related to T. tortugae McClendon, 1911, a species originally described from the Dry Tortugas, off southern Florida, USA, and later scarcely recorded from other western Atlantic localities, from Bermuda to Mexico and Brazil. Some clarification and additional illustrations are provided for the type material of T. tortugae. Typton jonkayei sp. nov., is described based on material from fouling-encrusting communities dominated by sponges, growing on submerged roots of the red mangrove, Rhizhophora mangle L., in Bocas del Toro, Caribbean coast of Panama. This new species differs from T. tortugae in several morphological details, for instance, on the minor and major chelipeds (second pereiopods), telson, uropod, frontal margin and ambulatory pereiopods. Typton cousteaui sp. nov. is described based on a single ovigerous female dredged in the southern Gulf of California off Baja California Sur, Mexico, previously reported as T. tortugae. This new taxon seems to represent a true cryptic species with no significant morphological divergence from the allopatrically isolated T. tortugae, except for slight morphometric differences. In addition, T. granulosus Ayón-Parente, Hendrickx & Galvan-Villa, 2015 is recorded from the Pacific coast of Panama, based on material collected in the Coiba Archipelago. Some taxonomic, distributional and ecological remarks are provided for T. granulosus and the closely related T. serratus Holthuis, 1951.

Intestinal microbes: an axis of functional diversity among large marine consumers

Microbes are ubiquitous throughout the world’s oceans, yet the manner and extent of their influence on the ecology and evolution of large, mobile fauna remains poorly understood. Here, we establish the intestinal microbiome as a hidden, and potentially important, ‘functional trait’ of tropical herbivorous fishes—a group of large consumers critical to coral reef resilience. Using field observations, we demonstrate that five common Caribbean fish species display marked differences in where they feed and what they feed on. However, in addition to space use and feeding behaviour—two commonly measured functional traits—we find that interspecific trait differences are even more pronounced when considering the herbivore intestinal microbiome. Microbiome composition was highly species specific. Phylogenetic comparison of the dominant microbiome members to all known microbial taxa suggest that microbiomes are comprised of putative environmental generalists, animal-associates and fish specialists (resident symbionts), the latter of which mapped onto host phylogeny. These putative symbionts are most similar to—among all known microbes—those that occupy the intestines of ecologically and evolutionarily related herbivorous fishes in more distant ocean basins. Our findings therefore suggest that the intestinal microbiome may be an important functional trait among these large-bodied consumers.

A Genus definition for Bacteria and Archaea based on a Standard Genome Relatedness Index

Genus assignment is fundamental in the characterization of microbes, yet there is currently no unambiguous way to demarcate genera solely using standard genomic relatedness indices. Here, we propose an approach to demarcate genera that relies on the combined use of the average nucleotide identity, genome alignment fraction, and the distinction between type- and non-type species. More than 3,500 genomes representing type strains of species from >850 genera of either bacterial or archaeal lineages were tested. Over 140 genera were analyzed in detail within the taxonomic context of order/family. Significant genomic differences between members of a genus and type species of other genera in the same order/family were conserved in 94% of the cases. Nearly 90% (92% if polyphyletic genera are excluded) of the type strains were classified in agreement with current taxonomy. The 448 type strains that need reclassification directly impact 33% of the genera analyzed in detail. The results provide a first line of evidence that the combination of genomic indices provides added resolution to effectively demarcate genera within the taxonomic framework that is currently based on the 16S rRNA gene. We also identify the emergence of natural breakpoints at the genome level that can further help in the circumscription of taxa, increasing the proportion of directly impacted genera to at least 43% and pointing at inaccuracies on the use of the 16S rRNA gene as a taxonomic marker, despite its precision. Altogether, these results suggest that genomic coherence is an emergent property of genera in Bacteria and Archaea.

Unesconia coibensis, gen. et sp. nov., a miniature sponge-associated shrimp from a biodiversity hotspot in the tropical eastern Pacific (Decapoda: Palaemonidae)

A new palaemonid shrimp genus, Unesconia gen. nov., is established to accommodate a peculiar, small, presumably sponge-associated species, Unesconia coibensis gen. et sp. nov. The description of the new genus and species is based on several specimens found in the shallow marine waters of the Coiba Archipelago, Pacific coast of Panama. Unesconia gen. nov. does not seem to have close affinities to other eastern Pacific or western Atlantic palaemonid genera, including those harbouring sponge symbionts. On the other hand, it shares many characters with three Indo-West Pacific genera, which contain sponge-associated species, viz. Paraclimenaeus Bruce, 1988, Apopontonia Bruce, 1976 and Climeniperaeus Bruce, 1996. The most important diagnostic features of Unesconia gen. nov. are the strongly carinate, dorsally dentate rostrum, with its lateral carinae greatly expanded basally and armed with strong supraorbital teeth; the non-filtering mouthparts, with mandible lacking palp; the first pereiopod chela with excavated fingers and strongly tridentate fingertips; the asymmetrical second pereiopods (chelipeds), with the major chela bearing a double-fossa mechanism on the finger cutting edges; the ambulatory pereiopod dactylus armed with one large tooth and at least two small spinules on the ventral margin of the corpus, in addition to the terminal unguis; the lateral section of the uropodal diaeresis armed with five spiniform setae, the latter not extending to the lateral margin of the exopod; and the telson with two pairs of stout long cuspidate setae on dorsal surface and three pairs of strong, elongate spiniform setae on the posterior margin.

A remarkable burrow-dwelling alpheid shrimp, new genus and new species, from the tropical eastern Pacific (Malacostraca: Decapoda: Caridea)

A new alpheid shrimp genus, Pachelpheus gen. nov., is established to accommodate Pachelpheus pachyacanthus sp. nov., described based on two specimens from the Las Perlas Archipelago, Pacific coast of Panama. Pachelpheus pachyacanthus sp. nov. appears to be an obligate symbiont dwelling in burrows of yet unknown infaunal hosts, on shallow near-shore subtidal sand flats. The main morphological characters of Pachelpheus gen. nov. are (1) frontal margin of carapace with broadly rounded rostral projection, without orbital teeth; (2) sixth pleonite with articulated plate; (3) telson with two pairs of cuspidate setae dorsally, without anal tubercles; (4) eyes concealed in dorsal view, partly visible in lateral view; (5) chelipeds equal in size, symmetrical in shape, moderately enlarged, stout, carried extended; (6) cheliped carpus without rows of setae mesially; (7) cheliped fingers without snapping mechanism, each finger armed with one stout tooth; (8) second pereiopod carpus with five sub-articles; (9) third, fourth and fifth pereiopods with ischia armed with single robust cuspidate seta, meri armed with one to several unusually robust cuspidate setae; (10) second pleopod with appendix masculina in males only; (11) uropodal exopod and endopod with rows of slender spiniform setae on their distal margins; (12) uropodal diaeresis unusually thickened laterally, with two very stout spiniform setae; and (13) lateral lobe of the uropodal protopod rounded. The new genus appears to be morphologically most similar to Jengalpheops (Anker & Dworschak, 2007) and Leslibetaeus (Anker, Poddoubtchenko & Wehrtmann, 2006).

Can interspecies affairs in the dark lead to evolutionary innovation?

Evolutionary adaptation is the adjustment of species to a new or changing environment. Engaging in mutualistic microbial symbioses has been put forward as a key trait that promotes the differential, evolutionary success of many animal and plant lineages (McFall‐Ngai, 2008). Microbial mutualists allow these organisms to occupy new ecological niches where they could not have persisted on their own or would have been constrained by competitors. Vertical transmission of beneficial microbial symbionts from parents to the offspring is expected to link the adaptive association between a given host and microbe, and it can lead to coevolution and sometimes even cospeciation (Fisher, Henry, Cornwallis, Kiers, & West, 2017). Vertical transmission also causes bottlenecks that strongly reduce the effective population size and genetic diversity of the symbiont population. Moreover, vertically transmitted symbionts are assumed to have fewer opportunities to exchange genes with relatives in the environment. In a “From the Cover” article in this issue of Molecular Ecology, Breusing, Johnson, Vrijenhoek, and Young (2019) investigated whether hybridization among different host species could lead to interspecies exchange of otherwise strictly vertically transmitted symbionts. Hybridization of divergent lineages can potentially cause intrinsic and extrinsic incompatibilities, swamp rare alleles, and lead to population extinctions. In some cases, however, it might also create novel trait combinations that lead to evolutionary innovation (Marques, Meier, & Seehausen, 2019). Breusing et al. (2019) linked the concept of hybridization to symbiont transmission, and their findings have significant implications for the study of evolution of vertically transmitted symbionts and their hosts.