Conflict, Competition, and Cooperation Regulate Social Interactions in Filamentous Fungi

Abstract

Social cooperation impacts the development and survival of species. In higher taxa, kin recognition occurs via visual, chemical, or tactile cues that dictate cooperative versus competitive interactions. In microbes, the outcome of cooperative versus competitive interactions is conferred by identity at allorecognition loci, so called kind recognition. In syncytial filamentous fungi, the acquisition of multicellularity is associated with somatic cell fusion within and between colonies. However, such intraspecific cooperation entails risks, as fusion can transmit deleterious genotypes or infectious components that reduce fitness, or give rise to cheaters that can exploit communal goods without contributing to their production. Allorecognition mechanisms in syncytial fungi regulate somatic cell fusion by operating precontact during chemotropic interactions, during cell adherence, and postfusion by triggering programmed cell death reactions. Alleles at fungal allorecognition loci are highly polymorphic, fall into distinct haplogroups, and show evolutionary signatures of balancing selection, similar to allorecognition loci across the tree of life. Expected final online publication date for the Annual Review of Microbiology, Volume 74 is September 8, 2020. Please see http://www.annualreviews.org/page/journal/pubdates for revised estimates.

The conserved serine transporter SdaC moonlights to enable self recognition

“…Molecular crosstalk mirrors observed interactions between nutrient availability, collective behavior, and self recognition in many organisms. Collective behaviors are associated with nutrient limitation in other microbes (Kundert & Shaulsky, 2019; Wall, 2014), fungi (Gonçalves et al, 2020), and plants (Palmer et al, 2016). Collective behaviors can allow for sharing of nutrients and promote developmental processes such as fruiting body formation.…”

“…For example, individual neurons express their identity through a unique set of clustered protocadherin proteins that interact between cells to inform neuronal self-avoidance and proper circuit formation (Kostadinov & Sanes, 2015; Lefebvre et al, 2012; Molumby et al, 2016). Kin cells of filamentous fungi can fuse to share resources in a syncytial lifestyle (Fischer & Glass, 2019; Gonçalves et al, 2020). And social microbes can identify, and coordinate with, kin during group migrations and fruiting body formation (Asfahl & Schuster, 2017; Gibbs et al, 2008; Gruenheit et al, 2017; Hirose et al, 2017; Pathak et al, 2013; Wenren et al, 2013).…”

Somatic deficiency causes reproductive parasitism in a fungus

“…Filamentous fungi form hyphae that branch and fuse regularly to form a dense, radially growing mycelial network [13][14][15] . Hyphal fusion is a costly somatic trait that pays off because it makes asexual spore production more efficient 16 .…”

A Nuclei-Based Conceptual Model of (Eco)evolutionary Dynamics in Fungal Heterokaryons

“…Naturally occurring heterokaryons of many species have been isolated, e.g., Cercospora musae ( Calpouzos, 1954 ), Aspergillus nidulans ( Jinks, 1952 ), Heterobasidion annosum ( Johannesson and Stenlid, 2004 ), Cryphonectria parasitica ( Milgroom et al, 2009 ), and Epichloë species ( Shoji et al, 2015 ). It was previously thought that heterokaryon formation is rare in nature due to heterokaryon incompatibility (HI), i.e., regulated cell death occurring at the place of fusion between the two hyphae of incompatible mycelia ( Glass and Dementhon, 2006 ; Daskalov et al, 2017 ; Gonçalves et al, 2020 ; Rico-Ramírez et al, 2022 ). Whilst this is not always the case ( Heller et al, 2018 ; Daskalov et al, 2019 ), evidence is accumulating that in spore germination phase, HI mechanisms may be relaxed or absent under different environmental conditions ( Roca et al, 2005 ; Ishikawa et al, 2012 ; Mehta and Baghela, 2021 ; Vangalis et al, 2021 ).…”