Ancient Rapid Radiation Explains Most Conflicts Among Gene Trees and Well-Supported Phylogenomic Trees of Nostocalean Cyanobacteria

Abstract

Prokaryotic genomes are often considered to be mosaics of genes that do not necessarily share the same evolutionary history due to widespread Horizontal Gene Transfers (HGTs). Consequently, representing evolutionary relationships of prokaryotes as bifurcating trees has long been controversial. However, studies reporting conflicts among gene trees derived from phylogenomic datasets have shown that these conflicts can be the result of artifacts or evolutionary processes other than HGT, such as incomplete lineage sorting, low phylogenetic signal, and systematic errors due to substitution model misspecification. Here, we present the results of an extensive exploration of phylogenetic conflicts in the cyanobacterial order Nostocales, for which previous studies have inferred strongly supported conflicting relationships when using different concatenated phylogenomic datasets. We found that most of these conflicts are concentrated in deep clusters of short internodes of the Nostocales phylogeny, where the great majority of individual genes have low resolving power. We then inferred phylogenetic networks to detect HGT events while also accounting for incomplete lineage sorting. Our results indicate that most conflicts among gene trees are likely due to incomplete lineage sorting linked to an ancient rapid radiation, rather than to HGTs. Moreover, the short internodes of this radiation fit the expectations of the anomaly zone, i.e., a region of the tree parameter space where a species tree is discordant with its most likely gene tree. We demonstrated that concatenation of different sets of loci can recover up to 17 distinct and well-supported relationships within the putative anomaly zone of Nostocales, corresponding to the observed conflicts among well-supported trees based on concatenated datasets from previous studies. Our findings highlight the important role of rapid radiations as a potential cause of strongly conflicting phylogenetic relationships when using phylogenomic datasets of bacteria. We propose that polytomies may be the most appropriate phylogenetic representation of these rapid radiations that are part of anomaly zones, especially when all possible genomic markers have been considered to infer these phylogenies.

Molecular diversity and evolution of far-red light-acclimated photosystem I

“…Given that these are single tree phylogenies, and that some of the smaller sequence alignments do not have high resolving power, it is still possible that these results can be explained by other phenomena such as incomplete lineage sorting of duplicated genes as a consequence of the rapid diversification process occurring around the initial divergence of micro-and macrocyanobacteria. This has been demonstrated recently for incongruences in gene and species trees within the heterocystous cyanobacteria (Pardo-De la Hoz et al, 2023) and is likely to affect other cyanobacterial relationships as well. Future analyses should also consider the conservation of gene synteny in the cluster across taxa and disparities in G+C content in the FaRLiP cluster relative to the rest of the genome to infer and single out HGT events more confidently.…”

Common Methods for Phylogenetic Tree Construction and Their Implementation in R

“…For a specific group of species, phylogenetic trees constructed from individual genes often show inconsistency with each other [61,62]. As the number of taxa increases, single-gene phylogenetic trees typically have low statistical support [63]. Studies have reported that when using the same parameters and the same program, approximately 9% to 18% of single-gene phylogenetic trees cannot replicate the same topology [64].…”

The underestimated fraction: diversity, challenges and novel insights into unicellular cyanobionts of lichens

“…Of the 24 cyanobiont genomes, 21 belong to Nostoc spp., with the remainder belonging to Rhizonema spp . [ 52 ]. However, the first attempts based on full genome data of free-living and lichenized Nostoc strains identified genes potentially involved in symbioses, which may help to improve taxonomic resolution [ 53 ].…”

“…The increased isolation efforts of INCb will expand the genomic data, and result in the first publicly available unicellular cyanobiont genome. Rapidly growing numbers of genome sequences of cyanobacteria provide an increasing amount of evidence that single genetic markers, several markers, or morphological data have only limited power when recognizing the diversity between and within species [ 52 , 54 ]. Additionally, it is likely that one lichen thallus can host several lineages of cyanobionts due to the potentially huge diversity at the genome level within single lineages of cyanobacteria [e.g.…”