Evolutionary significance of the microbial assemblages of large benthic Foraminifera

Abstract

Large benthic Foraminifera (LBF) are major carbonate producers on coral reefs, and are hosts to a diverse symbiotic microbial community. During warm episodes in the geological past, these reef-building organisms expanded their geographical ranges as subtropical and tropical belts moved into higher latitudes. During these range-expansion periods, LBF were the most prolific carbonate producers on reefs, dominating shallow carbonate platforms over reef-building corals. Even though the fossil and modern distributions of groups of species that harbour different types of symbionts are known, the nature, mechanisms, and factors that influence their occurrence remain elusive. Furthermore, the presence of a diverse and persistent bacterial community has only recently gained attention. We examined recent advances in molecular identification of prokaryotic (i.e. bacteria) and eukaryotic (i.e. microalgae) associates, and palaeoecology, and place the partnership with bacteria and algae in the context of climate change. In critically reviewing the available fossil and modern data on symbiosis, we reveal a crucial role of microalgae in the response of LBF to ocean warming, and their capacity to colonise a variety of habitats, across both latitudes and broad depth ranges. Symbiont identity is a key factor enabling LBF to expand their geographic ranges when the sea-surface temperature increases. Our analyses showed that over the past 66 million years (My), diatom-bearing species were dominant in reef environments. The modern record shows that these species display a stable, persistent eukaryotic assemblage across their geographic distribution range, and are less dependent on symbiotic photosynthesis for survival. By contrast, dinoflagellate and chlorophytic species, which show a provincial distribution, tend to have a more flexible eukaryotic community throughout their range. This group is more dependent on their symbionts, and flexibility in their symbiosis is likely to be the driving force behind their evolutionary history, as they form a monophyletic group originating from a rhodophyte-bearing ancestor. The study of bacterial assemblages, while still in its infancy, is a promising field of study. Bacterial communities are likely to be shaped by the local environment, although a core bacterial microbiome is found in species with global distributions. Cryptic speciation is also an important factor that must be taken into consideration. As global warming intensifies, genetic divergence in hosts in addition to the range of flexibility/specificity within host-symbiont associations will be important elements in the continued evolutionary success of LBF species in a wide range of environments. Based on fossil and modern data, we conclude that the microbiome, which includes both algal and bacterial partners, is a key factor influencing the evolution of LBF. As a result, the microbiome assists LBF in colonising a wide range of habitats, and allowed them to become the most important calcifiers on shallow platforms worldwide during periods of ocean warming in the geologic past. Since LBF are crucial ecosystem engineers and prolific carbonate producers, the microbiome is a critical component that will play a central role in the responses of LBF to a changing ocean, and ultimately in shaping the future of coral reefs.

Keywords: Cenozoic; climate change; coral reefs; microbiome; ocean warming; symbiosis.

Figure 1

Possible roles and relationships between large benthic Foraminifera and their algal symbionts and bacterial groups. Dinoflagellate‐bearing species are more dependent on their symbiont than diatom‐bearing and other algal‐bearing species for acquiring energy. Therefore, it is likely that species that rely less on algal symbiosis for growth and calcification utilise bacteria as a food source and require additional translocation of organic compounds from cyanobacteria. Bold arrows correspond to a high dependence on the exchange represented. Light grey arrows represent compounds being exchanged from the host to the microbial associate, whereas dark grey arrows represent the exchange from the microbial associate to the host.

Figure 2

Different species of large benthic Foraminifera host diverse algal symbiont communities. (A) Diatom‐bearing, dinoflagellate‐bearing and chlorophyte‐bearing species in sediment samples from Heron Island, southern Great Barrier Reef, Australia, represented by red, green, and blue arrows, respectively (scale bar = 0.5 cm). (B) Rhodophyte‐bearing Dendritina sp. (white arrow), and diatom‐bearing specimens of Operculina and Nummulites (red arrows) found in reefs off Spermonde Archipelago, Indonesia (scale bar = 1 cm). (C) Rhodophyte‐bearing Peneroplis planatus collected at Lizard Island, northern Great Barrier Reef, Australia (scale bar = 250 μm). (D) Specimens of Amphisorus sp. from Mindanao, Philippines, hosting symbiotic chlorophytes (green arrows) and dinoflagellates (blue arrows) (scale bar = 1 mm). (E) Diatom‐bearing Amphistegina lobifera and Amphistegina lessonii from the northern Great Barrier Reef, Australia (scale bar = 0.5 mm).

Figure 3

Modern global distribution of large benthic Foraminifera with algal symbionts, and average sea‐surface temperature. 1, Li et al. (1999); 2, Smith et al. (2001); 3, Albani (1978); 4, Betjeman (1969); 5, Orpin, Haig, & Woolfe (1999); 6, Parker (2009); 7, Narayan & Pandolfi (2010); 8, Michie (1987); 9, Heron‐Allen & Earland (1924); 10, Debenay (2012); 11, Kosciuch et al. (2018); 12, Todd (1965); 13, Collen & Garton (2004); 14, W. Renema, personal observation; 15, Langer & Lipps (2003); 16, Fujita et al. (2009); 17, Lessard (1980); 18, Makled & Langer (2011); 19, Hallock (1984); 20, Oki (1989); 21, Sugihara, Masunaga, & Fujita (2006); 22, Zheng & Zheng (1978); 23, Hallock & Glenn (1986); 24, Renema (2002); 25, Hoefker (1927); 26, Natsir & Subkhan (2012); 27, Renema & Troelstra (2001); 28, Renema (2003); 29, Renema (2008a); 30, Burollet et al. (1986); 31, Renema (2006a); 32, Natsir, Subkhan, & Wardhani (2012); 33, Jumnongthai (1980); 34, Jayaraju, Reddy, & Reddi (2011); 35, Muruganantham, Ragavan, & Mohan (2017); 36, Vedantam & Rao (1970); 37, Jayaraju & Reddi (1996); 38, Pisapia et al. (2017); 39, Parker & Gischler (2011); 40, Murray (1994); 41, Bhalla et al. (2007); 42, Rao (1971); 43, Pilarczyk et al. (2011); 44, Clarke & Keij (1973); 45, Parker & Gischler (2015); 46, Al‐Wosabi, Mohammed, & Al‐Kadasi (2011); 47, Hottinger (1980); 48, Karisiddaiah, Veerayya, & Guptha (1988); 49, Thissen & Langer (2017); 50, Zinke et al. (2005); 51, Langer et al. (2013a); 52, Haunold, Baal, & Piller (1997); 53, Hottinger, Halicz, & Reiss (1993); 54, Hyams, Almogi‐Labin, & Benjamini (2002); 55, Mouanga & Langer (2014); 56, Koukousioura, Dimiza, & Triantaphyllou (2010); 57, Hollaus & Hottinger (1997); 58, Triantaphyllou, Koukousioura, & Dimiza (2009); 59, Caruso & Cosentino (2014); 60, Langer et al. (2012); 61, El Kateb et al. (2018); 62, Pascual & Martín‐Rubio (2004); 63, Lévy et al. (1997); 64, Fajemila & Langer (2017); 65, McCulloch (1981); 66, Ebrahim (2000); 67, Cushman (1924); 68, Fajemila, Langer, & Lipps (2015); 69, Fujita & Omori (2015); 70, Bicchi, Debenay, & Pages (2002); 71, Whittaker & Hodgkinson (1995); 72, Yamano, Miyajima, & Koike (2000); 73, Baccaert (1987); 74, Renema, Beaman, & Webster (2013); 75, Jell, Maxwell, & McKellar (1965); 76, Mamo (2016); 77, Araújo & Machado (2008); 78, Barbosa et al. (2012); 79, Lévy et al. (1995); 80, Batista, Vilela, & Koutsoukos (2007); 81, Machado & Souza (2017); 82, Javaux & Scott (2003); 83, Cockey, Hallock, & Lidz (1996); 84, Culver & Buzas (1981); 85, Culver & Buzas (1982); 86, Al‐Wosabi, Mohammed, & Basardah (2017); 87, Murray (1974); 88, Förderer, Rödder, & Langer (2018); 89, Heron‐Allen & Earland (1915); 90, Cushman (1921); 91, Hayward et al. (1999).

Figure 4

The typical life cycle of large benthic Foraminifera showing potential routes for acquisition of algal symbionts and bacteria. During sexual reproduction gametes do not carry the algal symbionts, and symbionts are acquired horizontally. By contrast, algal symbionts are vertically acquired during asexual fission. It remains unclear if adults acquire algal symbionts and bacteria from the environment, and how bacteria are transferred from parents to offspring. Dashed black arrows denote uncertain routes of acquisition and the solid red arrow denotes a known transfer route.

Figure 5

Light penetration in oceanic and coastal waters, and the known vertical distribution of algal symbionts in large benthic Foraminifera.

Figure 6

Spindle plots showing the diversity of symbiont‐bearing taxa throughout the Cenozoic [ca. 40–2.6 million years ago (Ma)]. Some fossil large benthic foraminifera (LBF) genera found in the Caribbean have uncertain symbiont type.